Nabila Saleh-Subaie’s research while affiliated with National Autonomous University of Mexico and other places

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Publications (5)


Differences in AICc scores (ΔAICc) between each compet- ing model and the best-fitting model (indicated by ΔAICc = 0 and highlighted in bold) for three life-history traits of six fish species of the family Poeciliidae. Competing models represent that traits may vary among species and/or may be influenced by female size. The addition and multiplication symbols represent additive and interactive effects of predictors, respectively
Life histories of poeciliid fishes: searching for a size-dependent trade-off between number and size of offspring
  • Article
  • Full-text available

July 2023

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62 Reads

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1 Citation

Ichthyological Research

J. Jaime Zúñiga-Vega

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Nabila Saleh-Subaie

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A large body of knowledge about life-history traits has arisen from research on viviparous fishes of the family Poeciliidae. Still, the wide variation among species in reproductive strategies provides an excellent opportunity to further explore how life-history traits covary and the causes of covariation patterns. In this study, we provide information on brood size, offspring mass at birth, and total reproductive allotment of six poeciliid species ( Gambusia sexradiata , Poeciliopsis latidens , Poeciliopsis viriosa , Priapella intermedia , Pseudoxiphophorus jonesii , and Xiphophorus hellerii ). Also, we searched for a trade-off between the number of offspring that females produce and the size of each individual offspring. We tested the hypothesis that this trade-off should be stronger in small females because of the space constraints in the reproductive tract that are inherent to a small body size. If this hypothesis were correct, we expected a strong negative relationship between number and size of offspring in small females and a weaker or undetectable relationship between these two life-history traits in larger females. We found evidence of such a size-dependent trade-off in only one species. Small females of Po. latidens that produced relatively large broods experienced the cost of a reduction in the average size of each offspring. In larger females this negative relationship was weaker. Unexpectedly, we found no evidence of this trade-off in the other five poeciliid species and, in contrast, in one species ( Priapella intermedia ) females that produced numerous embryos were also capable of producing relatively large embryos. We discuss potential explanations for the different patterns of covariation (or lack of covariation) between number and size of offspring that we detected in these viviparous species.

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Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae

October 2022

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74 Reads

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2 Citations

The causes and consequences of the evolution of placentotrophy (post-fertilization nutrition of developing embryos of viviparous organisms by means of a maternal placenta) in non-mammalian vertebrates are still not fully understood. In particular, in the fish family Poeciliidae there is an evolutionary link between placentotrophy and superfetation (ability of females to simultaneously bear embryos at distinct developmental stages), with no conclusive evidence for which of these two traits facilitates the evolution of more advanced degrees of the other. Using a robust phylogenetic comparative method based on Ornstein–Uhlenbeck models of adaptive evolution and data from 36 poeciliid species, we detected a clear causality pattern. The evolution of extensive placentotrophy has been facilitated by the preceding evolution of more simultaneous broods. Therefore, placentas became increasingly complex as an adaptive response to evolutionary increases in the degree of superfetation. This finding represents a substantial contribution to our knowledge of the factors that have shaped placental evolution in poeciliid fishes.


(A) Lack of association between the matrotrophy index per population (MI) and average index of fullness (IFA) for 45 populations of five fish species from the genus Poeciliopsis. (B) Lack of association between the MI per population and the variance of the index of fullness among months (VarIFmonths) for 28 populations of three fish species from the genus Poeciliopsis.
Lack of association between the matrotrophy index per individual (MIind) and the individual index of fullness (IF) for 51 females of five fish species from the genus Poeciliopsis.
Lack of association between the MI per population and average body condition (BCA) for 45 populations of five fish species from the genus Poeciliopsis. Each species is shown in a different panel because of substantial differences among species in the values of body condition (BC). Each symbol represents a different species as per (Figures 1, 2).
Lack of association between the MI per population and the variance of body condition among months (VarBCmonths) for 28 populations of three fish species from the genus Poeciliopsis. Each species is shown in a different panel because of substantial differences among species in the values of BC. Each symbol represents a different species as per (Figures 1, 2).
Negative association between the MIind and individual BC for 51 females of five fish species from the genus Poeciliopsis. Each species is shown in a different panel because of substantial differences among species in the values of BC. Fitted lines represent model-averaged regression coefficients. Each symbol represents a different species as per (Figures 1, 2).
Examination of the Trexler-DeAngelis Model of Maternal Provisioning Reveals That Matrotrophy Is Costly

September 2021

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76 Reads

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4 Citations

The evolution of matrotrophy (post-fertilization maternal provisioning to developing embryos) has been explained through several hypotheses. Trexler and DeAngelis proposed in 2003 a theoretical model that defines the ecological conditions under which matrotrophy would be favored over lecithotrophy (pre-fertilization maternal provisioning). According to this model, matrotrophy offers a selective advantage in environments with abundant and constantly available food, whereas environments with limited and fluctuating food resources should instead promote a lecithotrophic mode of maternal provisioning. This model also proposes that matrotrophy entails the consequence of leaner reproductive females and in turn shorter lifespans. In this study, we examined the Trexler-DeAngelis model using data from 45 populations of five viviparous species from the fish genus Poeciliopsis (family Poeciliidae). We used the matrotrophy index (MI) as a measure of post-fertilization maternal provisioning, and the index of stomach fullness and individual body condition (BC) as proxies for food availability. We also estimated the magnitude of fluctuations in food availability by calculating the temporal variances of these two proxies. Neither abundant nor constantly available food were associated with greater degrees of matrotrophy, which fails to support the predictions of the Trexler-DeAngelis model with respect to the ecological drivers of increased post-fertilization provisioning to embryos. Nonetheless, in all five species we observed that females with greater degrees of matrotrophy had poorer BC compared to females that provided less nutrients to embryos after fertilization. This finding is consistent with one of the expected consequences of advanced matrotrophy according to the Trexler-DeAngelis model, namely, a detriment to the nutritional status of females. Our study provides compelling evidence that gestating females experience a trade-off between post-fertilization provisioning to embryos and self-maintenance, revealing in turn that matrotrophy is a costly reproductive strategy.


Changes in the mass of individual embryos as development progresses for small (white circles and dashed lines) and large (black circles and continuous lines) females. These two size categories correspond to females with a standard length below (small) or above (large) the population median. In these four populations we detected an interactive effect of female length and developmental stage on individual embryo mass. (a) Population 8 of Poeciliopsis infans: small females are matrotrophic whereas large females are lecithotrophic. (b) Population 2 of P. infans and (c) population 6 of P. turrubarensis. In these two populations, small females exhibit incipient matrotrophy whereas large females are predominantly lecithotrophic. (d) Population 3 of P. prolifica: small females exhibit a low degree of matrotrophy whereas large females are highly matrotrophic. In Fig. S1 we use three‐dimensional scatterplots to represent these same associations but using female length as a continuous variable.
Changes in the mass of individual embryos as development progresses for small (white circles and dashed lines) and large (black circles and continuous lines) females. These two size categories correspond to females with a standard length below (small) or above (large) the population median. In these 10 populations we detected an additive effect of female length and developmental stage on individual embryo mass. (a) Population 3 of Gambusia vittata, populations (b) 4 and (c) 11 of Poeciliopsis gracilis, populations (d) 2 and (e) 4 of P. latidens, populations (f) 5 and (g) 7 of P. prolifica, populations (h) 1, (i) 3, and (j) 4 of P. turrubarensis. In Fig. S2 we use three‐dimensional scatterplots to represent these same associations but using female length as a continuous variable.
Effects of female length on the number of simultaneous broods (i.e. degree of superfetation). Populations (a) 4, (b) 5, and (c) 11 of Poeciliopsis infans, (d) population 6 of P. prolifica, and (e) population 7 of P. turrubarensis.
Small sizes, big strategies: the relationship between female size, matrotrophy and superfetation throughout the reproductive lives of poeciliid fishes

July 2021

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33 Reads

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2 Citations

In viviparous fishes, females of species that exhibit matrotrophy (post‐fertilization maternal provisioning to developing embryos) and superfetation (ability of females to bear simultaneously multiple broods of embryos at distinct developmental stages) increase less in mass and volume during pregnancy than females of species that lack these traits. Such a reduction in reproductive allocation may provide greater benefits to young and small females for two reasons. First, they could devote energy and resources to both growth and reproduction. Second, they could compensate for the space restrictions that are inherent to a small body size because both superfetation and matrotrophy maximize fecundity for any given ovarian volume. In this study, we test the hypothesis that both matrotrophy and superfetation will decrease over female reproductive lifespan (i.e. as they grow larger). We examined reproductive females from 77 populations of 13 species of the family Poeciliidae. Remarkably, we found support for the matrotrophy prediction in only three populations. As expected, in these populations, small females were more matrotrophic than larger females, which in turn exhibited a predominantly lecithotrophic strategy. In one population, we found the opposite pattern—the degree of matrotrophy actually increased in larger females. With respect to superfetation, none of the populations showed a pattern consistent with our prediction. In fact, in five populations the pattern was opposite to our expectation—larger females produced more simultaneous broods than smaller females. Our findings reveal that the degree of matrotrophy and superfetation can vary throughout the adult lifespans of poeciliid fishes, but such ontogenetic shifts are not common in natural populations.

Citations (5)


... Schlupp 2011;Frías-Alvarez et al. 2014;Golden, Belk, and Johnson 2021;Hulthén et al. 2021;Jaime Zúñiga-Vega, Reznick, and Johnson 2007;Johnson and Belk 2001;José, Rodríguez, and León 2013;Mukherjee et al. 2014;Pollux et al. 2009;Reznick, Rodd, and Cardenas 1996;Reznick 1997;Reznick and Bryga 1996;Langerhans 2013, 2020;Riesch et al. 2014;Roth-Monzón et al. 2021;Schlupp, Taebel-Hellwig, and Tobler 2010;Weldele, Jaime Zúñiga-Vega, and Johnson 2014;Zúñiga-Vega et al. 2024). Pioneering work done in the Trinidadian guppy (Poecilia reticulata) Reznick and Endler 1982;Reznick 1997) has inspired dozens of additional research studies in several other livebearing fishes, each testing some aspect of life history theory. ...

Reference:

Standardized Approach to Life History Data Collection in Poeciliid Fishes
Life histories of poeciliid fishes: searching for a size-dependent trade-off between number and size of offspring

Ichthyological Research

... Thirteen hummingbird species inhabit Mexico City, one of the largest cities in the world (Puga-Caballero et al. 2020, Z uñiga-Vega et al. 2023. This study aims to evaluate how biological factors influence the local distribution of two hummingbird species in a remnant patch of native xerophytic scrubland embedded within the southern part of the city (Zambrano et al. 2016). ...

Raptors in the city: Site occupancy and abundance of a top predator inhabiting urban green spaces within a megacity
  • Citing Article
  • June 2023

Landscape and Urban Planning

... La familia está representada por aproximadamente 270 especies válidas (Fricke et al., 2020), cuya distribución en el continente americano comprende desde Estados Unidos hasta el Noreste de Argentina (Miller et al., 2005), pero su mayor diversidad ocurre en Centroamérica, México y las islas del Caribe (Rosen y Bailey, 1963). Todas las especies excepto una de esta familia son vivíparas, (Furness et al., 2019;Safian et al., 2023), ya que las hembras presentan fecundación interna por medio del gonopodio del macho, portando a los embriones en la gónada hasta su nacimiento (Torres-Martínez et al., 2023); las hembras son altamente fértiles, capaces de producir camadas sucesivas, esto debido a su capacidad de retener el esperma y presentar superfetación (Miller et al., 2005;de León-Gonzales, 2022), teniendo la capacidad de gestar simultáneamente dos o más grupos de embriones en diferentes etapas de desarrollo (García-Cabello, 2022). En embriones de peces el desarrollo osteológico es un proceso detallado que se inicia con la formación de cartílago y su posterior osificación (Rodríguez-Ibarra et al., 2017); considerando los trabajos osteológicos con poecílidos son escasos y se han centrado generalmente en áreas específicas del esqueleto, por ejemplo, Mookerjee & Mazumdar (1940) con la descripción del desarrollo de la columna vertebral de Lebistes reticulatus. ...

Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae

... Therefore, it is necessary to test, at the microevolutionary scale, whether the evolution of higher degrees of placentotrophy across populations of a given species promotes greater sexual conflict, which in turn promotes the evolution of enhanced strategies to ensure paternity, similar to the pattern that has been detected at the interspecific scale. The genus Poeciliopsis is characterized by variations between and within species in the degrees of female placentotrophy, where a positive relationship between the amount of maternal supply to developing embryos after fertilization and the degree of placental complexity has been confirmed (Turner 1940;Thibault and Schultz 1978;Reznick et al. 2002;Kwan et al. 2015;Olivera-Tlahuel et al. 2019;Molina-Moctezuma et al. 2020;Saleh-Subaie et al. 2021). Therefore, it is reasonable to hypothesize that, within Poeciliopsis species, males have also experienced phenotypic changes associated with greater post-copulatory sexual selection and sperm competition in populations in which females have evolved higher levels of placentotrophy. ...

Examination of the Trexler-DeAngelis Model of Maternal Provisioning Reveals That Matrotrophy Is Costly

... viriosa can also explain the occurrence of this trade-off only in Po. latidens because females of Po. viriosa are substantially larger (37.9 mm SL on average) than females of Po. latidens (24.0 mm SL on average; Table 2). A larger body size provides a larger reproductive cavity and, hence, less space restrictions for offspring production (Saleh-Subaie et al. 2021). ...

Small sizes, big strategies: the relationship between female size, matrotrophy and superfetation throughout the reproductive lives of poeciliid fishes