Girardinichthys Multiradiatus Research Articles

Genome biology of the darkedged splitfin, Girardinichthys multiradiatus, and the evolution of sex chromosomes and placentation.

Viviparity evolved independently about 150 times in vertebrates and more than 20 times in fish. Several lineages added to the protection of the embryo inside the body of the mother, the provisioning of nutrients, and physiological exchange. This often led to the evolution of a placenta. Among fish, one of the most complex systems serving the function of the placenta is the embryonal trophotaenia/ovarian luminal epithelium of the goodeid fishes. For a better understanding of this feature and others of this group of fishes, high-quality genomic resources are essential. We have sequenced the genome of the darkedged splitfin, Girardinichthys multiradiatus. The assembly is chromosome level and includes the X and Y Chromosomes. A large male-specific region on the Y was identified covering 80% of Chromosome 20, allowing some first inferences on the recent origin and a candidate male sex determining gene. Genome-wide transcriptomics uncovered sex-specific differences in brain gene expression with an enrichment for neurosteroidogenesis and testis genes in males. The expression signatures of the splitfin embryonal and maternal placenta showed overlap with homologous tissues including human placenta, the ovarian follicle epithelium of matrotrophic poeciliid fish species and the brood pouch epithelium of the seahorse. Our comparative analyses on the evolution of embryonal and maternal placenta indicate that the evolutionary novelty of maternal provisioning development repeatedly made use of genes that already had the same function in other tissues. In this way, preexisting modules are assembled and repurposed to provide the molecular changes for this novel trait.

Metabolic rate and hypoxia tolerance in Girardinichthys multiradiatus (Pisces: Goodeidae), an endemic fish at high altitude in tropical Mexico

The darkedged splitfin (Amarillo fish), Girardinichthys multiradiatus is a vulnerable endemic fish species inhabiting central Mexico's high altitude Upper Lerma Basin, where aquatic hypoxia is exacerbated by low barometric pressures (lower PO2s), large aquatic oxygen changes, poor aquatic systems management and urban, agricultural and industrial pollution. The respiratory physiology of G. multiradiatus under such challenging conditions is unknown - therefore the main goal of the present study was to determine metabolic rates and hypoxia tolerance to elucidate possible physiological adaptations allowing this fish to survive high altitude and increasingly eutrophic conditions. Fish came from two artificial reservoirs – San Elías and Ex Hacienda - considered refuges for this species. Both reservoirs showed high dial PO2 variation, with hypoxic conditions before midday and after 20:00 h, ~4 h of normoxia (15 kPa) from 16:00–20:00, and ~4 h of hyperoxia (16–33 kPa) from 12:00–16:00. Standard metabolic rate at 20 ± 0.5 °C of larvae from Ex Hacienda was significantly higher than those from San Elías, but these differences disappeared in juveniles and adults. Metabolic rate at 20 ± 0.5 °C for adults was 9.8 ± 0.1 SEM μmol O2/g/h. The metabolic scaling exponent for adults was 0.58 for San Elías fish and 0.83 for Ex Hacienda fish, indicating possible ecological effects on this variable. Post-larval fish in Ex Hacienda and all stages in San Elias site showed considerable hypoxia tolerance, with PCrit mean values ranging from 1.9–3.1 kPa, lower than those of many tropical fish at comparable temperatures. Collectively, these data indicate that G. multiradiatus is well adapted for the hypoxia associated with their high-altitude habitat.

Asymmetric paternal effect on offspring size linked to parent-of-origin expression of an insulin-like growth factor.

Sexual reproduction brings together reproductive partners whose long‐term interests often differ, raising the possibility of conflict over their reproductive investment. Males that enhance maternal investment in their offspring gain fitness benefits, even if this compromises future reproductive investment by iteroparous females. When the conflict occurs at a genomic level, it may be uncovered by crossing divergent populations, as a mismatch in the coevolved patterns of paternal manipulation and maternal resistance may generate asymmetric embryonic growth. We report such an asymmetry in reciprocal crosses between populations of the fish Girardinichthys multiradiatus. We also show that a fragment of a gene which can influence embryonic growth (Insulin‐Like Growth Factor 2; igf2) exhibits a parent‐of‐origin methylation pattern, where the maternally inherited igf2 allele has much more 5′ cytosine methylation than the paternally inherited allele. Our findings suggest that male manipulation of maternal investment may have evolved in fish, while the parent‐of‐origin methylation pattern appears to be a potential candidate mechanism modulating this antagonistic coevolution process. However, disruption of other coadaptive processes cannot be ruled out, as these can lead to similar effects as conflict.

Ichthyofauna in the XhimojayDam, State of Mexico

The State of Mexico has a large number of reservoirs that have the conditions necessary to host the life of freshwater fish, such is the case of Xhimojay dam for which there are no studies on the fish community. The objective of the present study was to determine the species of fish in the dam Xhimojay, State of Mexico, during the annual cycle 2013. Monthly samplings were made; the characteristics of habitat were recorded and collect organism for subsequent analysis in the laboratory. The physicochemical parameters which had a greater fluctuation in the system were deep and transparency. Four families were recorded where each family filed a species: Chirostoma jordani, Girardinichthys multiradiatus, Heterandria bimaculata and Cyprinus carpio, the most abundant species was G. multiradiatus with 1496 individuals and the species with smaller number of registered organisms was H. bimaculata with 121. The greatest diversity was presented in October and the lowest diversity was recorded in June. The species with the highest value of ecological importance was G. multiradiatus being that the physical and chemical parameters that characterize the environment favoring their presence.

Limited options for native goodeid fish simultaneously confronted to climate change and biological invasions

The process by which climate warming promotes the invasive expansion of tropical and sub-tropical species is commonly studied within the niche conservatism framework, which ignores the possibility of rapid evolution of thermal niche. We demonstrate that competition with the tropical invasive Pseudoxiphophorus bimaculatus has led to thermal niche displacement in the temperate fish Girardinichthys multiradiatus. Data mining of field records indicates that temperature is the main factor determining which species is dominant, behavioural performance profiles confirmed thermal segregation of these species and laboratory trials demonstrate that G. multiradiatus co-occurring with P. bimaculatus has shifted their thermal optimum to a lower temperature. An exploration of the consequences of these processes under climate change using a thermodynamic model predicts increased frequency of P. bimaculatus with global warming. This reveals a dilemma facing temperate species confronting tropical competitors; the need to adjust their thermal niche to escape competition behind a shrinking cold barrier, a lose–lose situation given current climatic trends.

La ecología alimentaria del pez endémico Girardinichthys multiradiatus (Cyprinidontiformes: Goodeidae), en el Parque Nacional Lagunas de Zempoala, México

Girardinichthys multiradiatus, locally known as "mexcalpique", is a small endemic fish of the Lerma river basin. Its presence in lakes (Zempoala) suggests a long-standing connection between these lakes and the river basin. The current range of this species in the Mexico and Toluca valley appears to have been reduced, making this park a refuge for the species. Nevertheless, little is known about its biology. We studied its diet and feeding habits in Acoyotongo Lake, Lagunas de Zempoala National Park (19 degrees 01'30"-19 degrees 06' N, 99 degrees 16'20"-99 degrees 21' W) where seasonal collections were carried out. The gut contents of 97 specimens were identified to the most specific taxonomic category possible and analyzed with numeric and frequency of occurrence methods. The general diet of this species consists of twelve dietary components, eleven of which are of animal origin. Hymenopterans, springtails and chironomids represented the highest percentage of ingestion and preference. G. multiradiatus is as a carnivorous species with entomophagous tendencies.

Congenital predispositions and early social experience determine the courtship patterns of males of the Amarillo fish

Mounting evidence indicates that learning shapes fish foraging and social behavior, which suggests that it may also underlie the frequently reported geographic variation in courtship. In this study, we analyzed how early social experience influences courtship patterns in males of the Amarillo fish (Girardinichthys multiradiatus). In a first experiment, we quantified the courtship of males from two allopatric populations grown in isolation and estimated the heritability of a key attribute of their courtship patterns. Then, we raised males from two allopatric populations with either sympatric or allopatric females and at two different densities, and registered their adult courtship patterns towards females from a third population. We found that the courtship pattern of males has a significant heritable component, yet in the second experiment, it was influenced by what type of females males were raised with, by their social rank (dominant/subordinate/singleton), and by the behavior of the female that they were courting. We conclude that courtship behavior in this fish has a congenital predisposition and is affected during development by different aspects of early experience and seemingly remains flexible throughout life; a complex ontogenetic trajectory that under natural conditions may have led to the locally stable dialect types observed in the courtship patterns of males from allopatric populations.

Female vibration discourages male courtship behaviour in the Amarillo fish (Girardinichthys multiradiatus)

Amarillo fish females (Girardinichthys multiradiatus) vibrate when conspecific males approach them; the reason behind this behaviour is unclear. Hypotheses are that females vibrate either to avoid aggression from males or to court them. We prevented females from vibrating by temporarily blocking their lateral line organs and eyes, on the assumption that they rely on these senses to detect approaching males. Females with the lateral line organs obstructed vibrated less frequently than females with the lateral line intact, indicating that the mechanosensory lateral line system is necessary for perceiving approaching males. Males displayed more courtship behaviour to sighted females with the lateral line organs obstructed than to sighted females with the lateral line intact. A general tendency indicated that the less the females vibrated the more the males courted them. These findings indicate that female vibration discourages male courtship behaviour.

Ecophysiological responses to the effect of annual management on an endemic viviparous fish in central plateau of Mexico

Studies on the biological aspects of fish typically focus on species that currently have commercial value, causing species that lack such market value to be ignored. This is the case of several freshwater fish, specifically of several members of the Goodeidae family. In the State of Querétaro there are several species of this family characterized for being viviparous and having distinctive sexual dimorphism that may have commercial potential. The subject of this study is Girardinichthys multiradiatus, a viviparous fish endemic to the upper-half of the Lerma River basin. The lack of knowledge regarding its biology and ecology has prevented the development of guidelines to manage its habitat and to preserve its population. The objective was to determine the ecophysiological responses of G. multiradiatus to its environmental management. From the sampling (24 hours every two months) population structure and dynamics were analyzed throughout a hydrological cycle using meristic data (standard length). Trophic and ecophysiological responses to fluctuations in environmental factors were also identified. Although the mexcalpique is a polytrophic species, results show that it prefers feeding on Diptera or Cladocera, while detritus is the third substance frequently found in their stomachs. Environmentally, the water regime is responsible for fluctuations in the population dynamics of the species, while temperature changes are the most influence its energy balance. These results can guide efforts to conserve this species and its habitat.

Reproductive Aspects of Yellow Fish Girardinichthys Multiradiatus (Meek, 1904) (Pisces: Goodeidae) in the Huapango Reservoir, State of Mexico, Mexico

The sexual maturity, age at first maturation and fecundity in females of the yellow fish Girardinichthys multiradiatus were analyzed in the Huapango reservoir located in the State of Mexico, Mexico. From July 2007 to May 2008 bimonthly samplings were carried out and, using a bait well net, 407 individuals were collected (245 females and 162 males). Overall, the sex ratio between females/males was 1.51:1 (P <0.05). The age of first maturation in the females was 33 mm of standard length. The spawning period occurred in July and accounted for the highest values in the gonadosomatic index. For the fertility model only fertilized eggs and embryos were considered, and those were adjusted to the potential model F=1E-08L5.6144 (P <0.05). This study contributes to the understanding of the reproductive biology of the yellow fish, which takes place in the reservoirs of the State of Mexico.

Reproduction and Survival Under Different Water Temperatures ofGyrodactylus mexicanus(Platyhelminthes: Monogenea), a Parasite ofGirardinichthys multiradiatusin Central Mexico

Gyrodactylid population growth may depend on abiotic variables such as temperature. We tested the survival and reproductive rate of Gyrodactylus mexicanus, a parasite infecting fins of Girardinichthys multiradiatus, at 3 different water temperatures, 10-13, 19-22, and 24 C. The temporal sequence of birth and age at death of each parasite isolated from the hosts was recorded through at least 8 generations. Our results showed that the average number of offspring per parasite was 2.0 when averaged across all temperatures. However, the generation time was negatively correlated with temperature. The innate capacity for increase (r(m)) was positively correlated with water temperature: from 0.29 parasite/day at 13 C to 0.48 parasite/day at 24 C. These data confirm that water temperature has a direct influence on parasite population dynamics. The current study represents the first contribution to understanding the population ecology of the monogenean G. mexicanus in central Mexico.

Variation in sexual dimorphism and assortative mating do not predict genetic divergence in the sexually dimorphic Goodeid fish Girardinichthys multiradiatus

Abstract Sexual dimorphism is often used as a proxy for the intensity of sexual selection in comparative studies of sexual selection and diversification. The Mexican Goodeinae are a group of livebearing freshwater fishes with large variation between species in sexual dimorphism in body shape. Previously we found an association between variation in morphological sexual dimorphism between species and the amount of gene flow within populations in the Goodeinae. Here we have examined if morphological differentiation within a single dimorphic species is related to assortative mating or gene flow between populations. In the Amarillo fish Girardinichthys multiradiatus studies have shown that exaggerated male fins are targets of female preferences. We find that populations of the species differ in the level of sexual dimorphism displayed due to faster evolution of differences in male than female morphology. However, this does not predict variation in assortative mating tests in the laboratory; in fact differences in male morphology are negatively correlated with assortative mating. Microsatellite markers reveal significant genetic differences between populations. However, gene flow is not predicted by either morphological differences or assortative mating. Rather, it demonstrates a pattern of isolation by distance with greater differentiation between watersheds. We discuss the caveats of predicting behavioural and genetic divergence from so-called proxies of sexual selection.

Female responsiveness underlies the evolution of geographic variation in male courtship between allopatric populations of the fish Girardinichthys multiradiatus

Traditionally, the origin of new species from disjoint populations has been thought to be due to the accumulation of mutations, genetic drift, or to local, divergent adaptation. It has also been proposed that sexual selection can accelerate, or even generate, reproductive isolation. Although there is some evidence that female choice is strong enough to generate reproductive isolation, the mechanism by which isolation is produced is still poorly understood. Here we show that (1) the population-characteristic male courtship behaviour of the amarillo fish (Girardinichthys multiradiatus, Meek) is modified in the presence of females from other populations, that (2) this is due to the males responding to subtle cues from females, but that (3) the resulting courtship style does not match the female’s population-characteristic behaviour. We conclude that the interplay between male courtship and female responsiveness has led to the evolution of local variants in courtship style that hamper communication between allopatric individuals and promote pre-mating isolation.

Two New Species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae) Parasitizing Girardinichthys multiradiatus (Cyprinodontiformes: Goodeidae), an Endemic Freshwater Fish from Central Mexico

Gyrodactylus mexicanus n. sp. and Gyrodactylus lamothei n. sp. are described from the fins and skin of Girardinichthys multiradiatus, an endemic freshwater fish from central Mexico. Gyrodactylus mexicanus is compared to other Gyrodactylus species that parasitize Fundulus spp., the phylogenetically closest group to the Goodeidae from North America. Gyrodactylus mexicanus is distinguished by having large anchors with well-developed superficial roots, enlarged hooks with a proximally disrupted shank (ligament), and a ventral bar with 2 poorly developed anterolateral projections and a small medial process. Gyrodactylus lamothei is distinguished from G. mexicanus and from other species of Gyrodactylus on the North American continent by having anchors with a sclerite on the superficial root and robust hooks with a straight shaft and a recurved point.

Courtship plasticity reveals the evolution of dialects in allopatric fish populations

AbstractTraditionally, reproductive isolation between disjoint populations has been thought to emerge as a result of the accumulation of different mutations, genetic drift, or through the effects of natural and sexual selection^1^. Alternatively, the ability of an organism to express different phenotypes depending on the environment (i.e. phenotypic plasticity) could produce reproductive isolation^2,3^. Sexually selected traits are expected to be phenotypically plastic and can result in modifications of the species recognition system and thus originate new species^4^. Here we show that the population-characteristic male courtship behaviour of a fish (Girardinichthys multiradiatus) is modified in the presence of females from other populations, that this is due to the males responding to subtle cues from females, and that they fail to emulate the female&amp;apos;s population-characteristic behaviour. We conclude that plasticity has led to the creation of local dialects in the courtship pattern that hampers communication between heterogametic individuals and promotes pre-mating isolation.

Effects of methyl parathion exposure on development and reproduction in the viviparous fish Girardinichthys multiradiatus

Methyl parathion (MeP), an insecticide commonly used in Mexico, has been detected in water bodies adjacent to agricultural crops and is accumulated in the tissue of the amarillo (Girardinichthys multiradiatus), a viviparous fish unique to Central Mexico. Evidence of MeP accumulation in a G. multiradiatus population prompted assessment of the consequences of exposure to MeP during the gestation period and adult life. We exposed adult fish to MeP in the diet at concentrations ranging from 0.001 to 0.165 microg/g dry weight of food. Fish accumulated MeP at concentrations from 0.21 to 5.87 microg/g of fish and exhibited a significant reduction in weight and growth rate. We also evaluated the effects on broods of pregnant females exposed to 0.005, 0.01, and 0.1 microg/g dry weight of food. Although these pregnant females were not affected, their offspring showed an increase in spinal cord malformation and a reduction in survival to adulthood. Finally, we sampled seven localities inhabited by G. multiradiatus; this revealed the presence of MeP in two water bodies at concentrations of 0.0036 and 0.037 microg/mL respectively. Our results suggest that low MeP concentrations affect immature fish with possible consequences later in life.

Exposure to pesticides impairs the expression of fish ornaments reducing the availability of attractive males

Ornament magnitude often reflects a local balance between sexual selection and other sources of natural selection opposing their elaboration. Human activity may disrupt this balance if it modifies the costs of producing, maintaining or displaying the ornaments. When costs are increased, a shortage of acceptable partners may ensue, with consequences commensurate with how stringent (and effective) the process of mate choice is. Here, we show that the expression of ornaments in the viviparous amarillo fish (Girardinichthys multiradiatus) is influenced by embryonic exposure to low concentrations of an organophosphorus insecticide. Male ornamental fin size, dimorphic yellow coloration and display rates were all compromised in exposed fish, but unaffected in their paternal half-sibling controls and in their sisters (morphology and colour). Exposure resulted in smaller fish of both sexes, thus the differential effect by sex was restricted to attributes such as fin size only above the naturally selected magnitude shown by females. Father phenotype predicted offspring morphology of controls, but not of exposed males, which were discriminated against by both control and exposed females. Since stringent female mate choice can result in females refusing to mate with suboptimal mates, this sub-lethal developmental effect can reduce the effective population size of amarillo fish populations.

Phenotypic differentiation and pre-mating isolation between allopatric populations of Girardinichthys multiradiatus

Sexual selection may lead to reproductive isolation between populations through divergence in female mate choice, and population differentiation driven by female mate choice is expected to produce pre- but not post-mating isolation. We tested these hypotheses by looking at whether allopatric populations of the Amarillo (Girardinichthys multiradiatus), a sexually dimorphic viviparous fish with effective female choice, (i) have undergone phenotypical differentiation that may be attributed to divergence in female mate choice, and (ii) are already separated by pre- and/or post-mating reproductive barriers. We found substantial divergence in morphological traits which are the target of female mate choice, and in male courtship behaviour. Strong female preferences for homogametic males indicate substantial and symmetric pre-copulatory isolation, but the few successful heterogametic crosses produced in confinement yielded litters of the same size as those produced in homogametic matings, suggesting that post-copulatory isolation between populations is non-existent or weak. It appears that the studied populations have undergone incipient speciation with a pattern that is consistent with speciation driven by sexual selection, yet further work should assess whether divergence in female preferences has promoted male phenotypic differentiation or whether variation in male attributes has driven divergence in female preferences.

A cost worth paying: energetically expensive interactions with males protect females from intrasexual aggression

When approached by males, females of the Amarillo fish (Girardinichthys multiradiatus) perform a behaviour called vibration or they are aggressively challenged. We quantified vibration and assessed whether it compromises the rate of feeding attempts in dyads kept in outdoor enclosures. Male approaches resulted in female vibration and in a reduced feeding rate. Vibration was not evoked by female–female aggression, which was frequent and always ended in the subordinate fleeing from the dominant female. Using a closed respirometer we found that vibration is costly; oxygen consumption of females was greater in the presence of a male (which evoked vibration) than in the presence of a non-familiar female (when no vibration occurred). By recording interactions of females confined in aquaria in the presence and in the absence of males, we confirmed that escaping is the only available response to deal with female aggression. Females kept without males participated in frequent aggressive (even lethal) interactions that did not abate while the subordinate female was in sight of the dominant, and which caused premature births and injuries. Yet in the alternative treatment aggression ceased when a male approached, prompting vibration in both females. Thus, in the Amarillo, in as much as it evokes energetically costly female vibrations, male courtship is an expression of sexual conflict. However, in the absence of males, frequent female aggression potentially annuls the benefits of not vibrating. We propose that a complete appraisal of the consequences of sexual conflict must include an assessment of the costs imposed by intra-sexual interactions.

Sperm Competition in a Viviparous Fish

We investigated multiple paternity and sperm precedence in the Amarillo fish, Girardinichthys multiradiatus (Goodeidae). We allowed females to mate with two different-sized males consecutively and assessed the paternity of the ensuing broods using allozyme electrophoresis. We presented one-half of the females the larger, and the other half the smaller, male first. Allozyme variation among individuals was low, yielding conservative estimates of multiple paternity. Half the broods were of mixed paternity, but one male always sired more than 70% of the embryos in each brood. The proportion of the brood sired was not related to mating sequence, but when we classified males by relative size, the larger male of each pair usually fathered greater proportions of offspring than the smaller male. This association disappeared when we used the actual size of the males in the analysis. Instead, for any pair of males, the difference in number of offspring sired was correlated to differences in the rate of courtship displays, rather than size differences, suggesting that courtship intensity is a better predictor of paternity than male size. Within a pair, the larger male usually displayed more than the smaller one, but there was no correlation between male size and display rate across all males. Parsimony suggests a correlation between courtship rate and sperm production, but we cannot rule out the possibility that females allocate paternity according to the relative merits of the males.