The evolution of placentas and superfetation in the fish genus Poecilia (Cyprinodontiformes: Poeciliidae: subgenera Micropoecilia and Acanthophacelus)

Complex adaptations are often found in nature, although our ability to discern how and why such traits evolved is limited because their origin occurred in the distant past and the details of their evolution have been lost through extinction (e.g. all placental mammals inherited their placentas from a single common ancestor that lived over 100 Mya). In poeciliid fishes, placentas have evolved independently multiple times and portions of the path to the evolution of complexity can be found in living species. In the present study, we describe the life histories of six species within the genus Poecilia that includes the subgenera Micropoecilia and Acanthophacelus (the guppy; Poecilia reticulata). We demonstrate that extensive placentotrophy and superfetation, the ability to simultaneously carry more than one developing brood, have evolved within this clade. These fish represent the third clade in which we have discovered the independent origin of a placenta that also includes close relatives that lack a placenta. We discuss possible adaptive advantages of the joint evolution of extensive placentation and superfetation in these fishes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 784–796.     

Predation and life-history variation in Poecilia reliculata (Cyprinodontiformes: Poeciliidae)

Synopsis Reznick and Endler investigated natural variation in life-history traits of populations of Trinidad guppies exposed to one of three intensities of predation: (i) high predation directed primarily at adults, (ii) moderate predation directed primarily at juveniles, and (iii) low predation. They were able to document significant interpopulational differences in life-history traits associated with this differential predation on a trait-by-trait basis. However, the present extended multivariate analysis indicates that (1) life-history traits do not differ significantly between populations exposed to moderate versus low predation, although both differ greatly from high-predation populations; (2) life-history variation is strongly unifactorial; and (3) despite the importance of predation effects, approximately 17% of the variation in life-history variables cannot be accounted for by predation intensity. Residual variation has no obvious geographical patterns, but instead seems to reflect local environmental variability. Life-history differences between predation regimes are consistent with residual patterns of variation within regimes, suggesting that local variation provides the raw material for extrapolation in response to predation, but also that it influences the direction of correlated change in life-history traits.     

Embryonic development and nourishment in the viviparous fish Poecilia vivipara (Cyprinodontiformes: Poeciliidae)

While viviparity confers protection to the embryos during gestation, it increases energetic costs for the mother, which acquires new relations to its offspring. Maternal–fetal transfer of nutrients can occur in different patterns: as lecithotrophy (nourished by yolk) or matrotrophy (nourished by the mother). The development of Poecilia vivipara embryos was described macroscopically and microscopically, and the form of nutritional provisioning was identified. Embryonic development was divided into three prefertilization and seven postfertilization stages. The first organ to appear is the notochord, followed by the nervous, digestive and cardiovascular systems, and then by muscles and eyes. Embryonic nutritional provisioning was lecithotrophic, with yolk persisting until the last developmental stages and rich in proteins and polysaccharides. This kind of embryonic nutrition confirms the pattern found in the family Poeciliidae.     

Comparative phylogeography of livebearing fishes in the genera Poeciliopsis and Poecilia (Poeciliidae: Cyprinodontiformes) in central Mexico

Aim To test the hypothesis that the vicariant event responsible for north–south divergences in two clades of the fish genus Poeciliopsis Regan was also responsible for north–south divergences in the fish Poecilia butleri Jordan. Location Central Mexico. Methods Parsimony, distance, maximum likelihood and Bayesian phylogenetic analyses of a mitochondrial gene. Molecular clock test and Bayesian analyses of divergence time. Results We report concordant phylogeographical patterns between two clades in the genus Poeciliopsis (i.e. the other formed by P. latidens Garman and P. fasciata Meek, and the other formed by P. presidionis Jordan and P. turneri Miller) and the clade of Poecilia butleri, with northern and southern individuals within each clade grouping into separate lineages. There is also evidence for slower substitution rates in Poecilia compared with Poeciliopsis. After taking into account these substitution rate discrepancies with Bayesian relaxed molecular clock analyses, north–south divergences in Poecilia butleri were equivalent to those reported for Poeciliopsis latidens‐fasciata and P. presidionis‐turneri. Main conclusions The same Plio‐Pleistocene vicariant event associated with geological activity of the Trans‐Mexican Volcanic Belt (TMVB) appears to have caused divergence in three different freshwater fish lineages. This study is an example of how comparative phylogeography can strengthen inferences about vicariant events in regions of high biological diversity and complex geological history such as the TMVB.     

Historical biogeography of the livebearing fish genus Poeciliopsis (Poeciliidae: Cyprinodontiformes)

To assess the historical biogeography of freshwater topminnows in the genus Poeciliopsis, we examined sequence variation in two mitochondrial genes, cytochrome b (1140 bp) and NADH subunit 2 (1047 bp). This widespread fish genus is distributed from Arizona to western Colombia, and nearly half of its 21 named species have distributions that border on the geologically active Trans-Mexican Volcanic Belt (TMVB), a region that defines the uplifted plateau (Mesa Central) of Mexico. We used the parametric bootstrap method to test the hypothesis that a single vicariant event associated with the TMVB was responsible for divergence of taxa found to the north and south of this boundary. Because the single-event hypothesis was rejected as highly unlikely, we hypothesize that at least two geological events were responsible for divergence of these species. The first (8-16 million years ago) separated ancestral populations that were distributed across the present TMVB region. A second event (2.8-6.4 million years ago) was associated with northward dispersal and subsequent vicariance of two independent southern lineages across the TMVB. The geological history of this tectonically and volcanically active region is discussed and systematic implications for the genus are outlined.     

An early stage of ZW/ZZ sex chromosome differentiation in Poecilia sphenops var. melanistica (Poeciliidae,Cyprinodontiformes)

The mitotic and meiotic chromosomes of the American cyprinodont fish Poecilia sphenops var. melanistica were analysed. All 46 chromosomes are telocentric. By specific staining of the constitutive heterochromatin with C-banding and various AT-specific fluorochromes, the homomorphic chromosome pair 1 could be identified as sex chromosomes of the ZW/ZZ type. All female animals exhibit a W chromosome with a large region of telomeric heterochromatin that is not present in the Z chromosome. These sex chromosomes cannot be distinguished by conventional staining; they represent the first demonstration of sex chromosomes in fishes in an early stage of morphological differentiation. The W heterochromatin and the telomeric heterochromatin in the two autosomes 18 show a very bright fluorescence when stained with AT-specific fluorochromes. This allows the direct identification of the chromosomal sex by examining the interphase nuclei: females exhibit three, males only two brightly fluorescent heterochromatic chromocenters in their nuclei. The significance of these ZW/ ZZ sex chromosomes and their specific DNA sequences, the dose compensation of the Z-linked genes, and the experimental possibilities using sex-reversed ZW males are discussed.     

Temperature tolerance polygon of Poecilia sphenops Valenciennes (Pisces: Poeciliidae)

1. The critical thermal maximum (CTMax) and minimum (CTMin), the upper and lower incipient lethal temperature, and the high and low avoidance temperature of Poecilia sphenops were established.2. The area of thermal tolerance of P. sphenops upon considering the lethal limits was 863.9 (°C)², the estimated area using the critical temperatures, as well as the zone of thermal preference were 959 and 323.4 (°C)², respectively.3. P. sphenops is a species highly eurythermical that possesses a high tolerance, resistance and capacity of adaptation to environmental variations.     

Responses to Light in Epigean and Hypogean Populations of Gambusia Affinis (Cyprinodontiformes: Poeciliidae)

The responses to light among the fish Gambusia affinis, permanent residents of hypogean brackish water basins of the Spunnulate dolinas system of Torre Castiglione, in southeastern Italy, were studied at light intensities of 180 and 430 lux. These fish showed, on the average, a negative phototactic behaviour (scotophilia) with a low coefficient of variability. On the other hand, epigean, spring-dwelling individuals of G. affinis from the same region showed a positive phototactic behaviour with a greater variability in the responses when compared with cave-dwelling conspecifics. Possible causes for the detachment of hypogean from epigean forms are discussed.     

Sexual and Aggressive Behaviour in Species Hybrids of Poecilia mexicana and Poecilia velifera (Pisces,Poeciliidae)

The inheritance of sexual behaviour patterns was studied in species hybrids of Poecilia mexicana and Poecilia velifera. In addition, the aggressive behaviour and some morphological characters have been investigated and checked for a possible correlation between and within these three different traits studied. All the characters are inherited polygenically. The minimum genetic factors could be estimated only for some characters.     

Phylogeography and monophyly of the swordtail fish species Xiphophorus birchmanni (Cyprinodontiformes, Poeciliidae)

We used sequences of the mitochondria control region to assess the distribution of genetic variation within and among populations of the poeciliid fish species Xiphophorus birchmanni . We collected 122 X. birchmanni samples from 11 sites in three drainage systems comprising the distribution of the species. We found low levels of polymorphism among aligned sequences and low levels of genetic variation within populations but high levels of genetic differentiation among populations. Haplotypes are exclusive to three river drainages (Los Hules, Calabozo and San Pedro). Mantel tests revealed correlations between geographical (both straight-line and river distances) and genetic distance, consistent with an isolation by distance scenario, while nested clade analysis suggested allopatric fragmentation between haplotypes from two of the major drainages, and isolation by distance with restricted gene flow within those drainages. Finally, monophyly of X. birchmanni is strongly supported while the previous hypothesis of the evolutionary origin of this species from X. malinche is not.     

Comparative morphology,phylogenetic relationships,and historical biogeography of plesiolebiasine seasonal killifishes (Teleostei: Cyprinodontiformes: Rivulidae)

Phylogenetic and biogeographical analyses were performed for the Plesiolebiasini, a group of 20 small and rare species of South American annual killifishes, some threatened with extinction, occurring in river basins of Brazil, Bolivia, Paraguay, and Argentina. The results of a maximum parsimony analysis of 142 morphological characters highly corroborate monophyly of the Plesiolebiasini. Monophyly of each plesiolebiasine genus is supported and Plesiolebias is hypothesized to be the sister group to a clade comprising the remaining plesiolebiasine genera (Papiliolebias, Pituna, Maratecoara, and Stenolebias), corroborating studies based on mitochondrial genes. The phylogenetic analysis supports sister group relationships between Papiliolebias and the clade containing Pituna, Maratecoara, and Stenolebias, and between Maratecoara and Stenolebias. The biogeographical analysis indicates a complex historical biogeographical scenario for plesiolebiasines. A vicariance event between the western Paraguay area and northern river basins may be related to the isolation of the Chaco region from the Amazon between the Late Oligocene and Early Miocene. A vicariance event involving the Paraguay River basin and northern rivers, and the multiple occurrence of area hybridism along the Araguaia depression are tentatively identified as a consequence of tectonic subsidence events occurring during the Pleistocene. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 131–148.     

Genetic variation and phylogeography of the swordtail fish Xiphophorus cortezi (Cyprinodontiformes, Poeciliidae)

Swordtail fish have been studied extensively in relation to diverse aspects of biology; however, little attention has been paid to the patterns of genetic variation within and among populations of swordtails. In this study, we sequenced the mtDNA control region from 65 individuals and 10 populations of Xiphophorus cortezi to investigate the genetic variation within and among populations, including tests for correlations between genetic and geographic distances and tests for species monophyly. We found low gene and nucleotide diversity within populations and high degrees of genetic differentiation among populations. Significant and positive correlations between genetic distance and both river and straight-line geographic distance indicate that genetic differentiation among X. cortezi populations can be explained, to some extent, by an isolation-by-distance model and provide evidence of stream capture. Phylogenetic analyses suggest that X. cortezi is paraphyletic relative to X. malinche, raising questions concerning the status of these taxa as separate species.     

Photophilic behaviour in surface- and cave-dwelling Atlantic mollies Poecilia mexicana (Poeciliidae)

The phototactic behaviour of surface- and cave-dwelling Atlantic mollies Poecilia mexicana was examined. Surface-dwelling Atlantic mollies, as well as light- and dark-reared cave fish showed photophilic behaviour under all light intensities used (620, 50 and 3 lx).     

A new and morphologically distinct population of cavernicolous Poecilia mexicana (Poeciliidae: Teleostei)

The cave molly, Poecilia mexicana, from the Cueva del Azufre, a sulfur cave in Tabasco, Mexico, ranks among the best-studied cave fishes worldwide, despite being known from a single population only. Here we describe a newly discovered second population of cave-dwelling P. mexicana from a nearby, but mostly non-sulfidic cave (Luna Azufre). Despite apparent similarities between the two populations (such as reduced eye diameter and reduced pigmentation), a geometric morphometric analysis revealed pronounced morphological differentiation between the two cave forms.     

Molecular phylogeny of the livebearing Goodeidae (Cyprinodontiformes)

The Goodeinae is a speciose group of viviparous freshwater fishes endemic to the Mesa Central of Mexico. The current taxonomy of the group is based on morphology associated with viviparity and several of the groupings are questionable. We sequenced part of the mitochondrial cytochrome c oxidase subunit I (COI) gene (627bp) and control region (approximately 430bp aligned) of representatives of 36 species (all genera) of goodeid fishes in order to establish phylogenetic relationships among the taxa. Findings support the monophyly of the Goodeidae, the sister-group relationship of the Empetrichthyinae and Goodeinae, and the relationship of Profundulus to the Goodeidae. All goodeine genera but Xenotoca were recovered as monophyletic. Many of the higher-level relationships within the group contradict the findings of previous studies based upon morphology. The rate of molecular change in COI (0.9% per Myr), calibrated with the fossil record and geological data, suggests an approximate age for the Goodeidae of 16.5Myr. The majority of divergence within the Goodeinae appears to have occurred during the Miocene, with subsequent cladogenesis in the Pliocene and Pleistocene. Most recent speciation appears allopatric. River piracy, particularly involving the Rio Ameca basin, has played a significant role in the diversification of the Goodeinae.     

Molecular systematics of the genus Allodontichthys (Cyprinodontiformes: Goodeidae)

Phylogenetic analyses of cytochrome c oxidasesubunit I (627bp) and mitochondrial controlregion (338bp aligned) sequences for all knownspecies of Allodontichthys wereperformed. Allodontichthys was recoveredas monophyletic, and A. hubbsi wassupported as the most primitive member of thegenus in all analyses. Combined-data analysessuggest that A. polylepis is sister to aclade comprising A. tamazulae and A. zonistius; however, a strict consensus of COIand control region cladograms results in acollapse of this node. The two species thatare broadly sympatric, A. hubbsi and A. tamazulae, are not sister taxa.Allodontichthys was found the sistergroup of a clade including Ilyodon andXenotaenia. These three genera are theonly goodeids to occupy high-gradient riversystems. Ilyodon and Allodontichthys share similar distributions;however, Allodontichthys exhibits greaterthan an order of magnitude more geneticvariation in COI than Ilyodon incomparisons of individuals from the samelocalities in the Ameca and Armeria drainagesystems. This is interpreted to mean Allodontichthys arrived in some westerndrainages significantly before Ilyodon.The Rio Coahuayana appears to be the center oforigin of the genus Allodontichthys. This river basin contains the most primitivemember of the genus, and appears to haveconnected with the Mesa Central, the center of endemism of the Goodeidae. A calibrated rateof molecular change in COI reveals Allodontichthys began diverging approximately6.2 million years ago (mya). Remainingspeciation in the group appears to haveoccurred about 2.7 to 3.3 mya. The hypothesisthat a hard polytomy comprising A. zonistius, A. polylepis, and A. tamazulae could be explained by speciation ofA. polylepis and A. tamazulae fromdifferent A. zonistius ancestors ispresented. Stream capture is evident but notfrequent in the history of Allodontichthys, and speciation does notclearly correlate with documented geologicactivity of the Mexican Transvolcanic Belt.