Vomeronasal organ volume increases with body size and is dissociated with the loss of a visual signal in Sceloporus lizards.

Many organisms communicate using signals in different sensory modalities (multicomponent or multimodal). When one signal or component is lost over evolutionary time, it may be indicative of changes in other characteristics of the signalling system, including the sensory organs used to perceive and process signals. Sceloporus lizards predominantly use chemical and visual signals to communicate, yet some species have lost the ancestral ventral colour patch used in male-male agonistic interactions and exhibit increased chemosensory behaviour. Here, we asked whether evolutionary loss of this sexual signal is associated with larger vomeronasal organ (VNO) volumes (an organ that detects chemical scents) compared with species that have retained the colour patch. We measured VNO coronal section areas of 7-8 adult males from each of 11 Sceloporus species (4 that lost and 7 that retained the colour patch), estimated sensory and total epithelium volume, and compared volumes using phylogenetic analysis of covariance, controlling for body size. Contrary to expectations, we found that species retaining the ventral patch had similar relative VNO volumes as did species that had lost the ancestral patch, and that body size explains VNO epithelium volume. Visual signal loss may be sufficiently compensated for by increased chemosensory behaviour, and the allometric pattern may indicate sensory system trade-offs for large-bodied species.

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

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.

Evolutionary loss of a signalling colour is linked to increased response to conspecific chemicals.

Behavioural responses to communicative signals combine input from multiple sensory modalities and signal compensation theory predicts that evolutionary shifts in one sensory modality could impact the response to signals in other sensory modalities. Here, we conducted two types of field experiments with 11 species spread across the lizard genus Sceloporus to test the hypothesis that the loss of visual signal elements affects behavioural responses to a chemical signal (conspecific scents) or to a predominantly visual signal (a conspecific lizard), both of which are used in intraspecific communication. We found that three species that have independently lost a visual signal trait, a colourful belly patch, responded to conspecific scents with increased chemosensory behaviour compared to a chemical control, while species with the belly patch did not. However, most species, with and without the belly patch, responded to live conspecifics with increased visual displays of similar magnitude. While aggressive responses to visual stimuli are taxonomically widespread in Sceloporus, our results suggest that increased chemosensory response behaviour is linked to colour patch loss. Thus, interactions across sensory modalities could constrain the evolution of complex signalling phenotypes, thereby influencing signal diversity.

Steroid hormones, ectoparasites, and color: Sex, species, and seasonal differences in Sceloporus lizards.

Testosterone, in addition to promoting the expression of sexual ornaments can negatively affect immune function, leaving individuals more susceptible to parasites (immunocompetence handicap hypothesis). Immunosuppressive effects of testosterone also can occur indirectly, through increased glucocorticoid hormones (corticosterone, cortisol). Therefore, the expression of sexual ornaments and the ability to respond to parasites and diseases may be influenced by the interaction between testosterone and corticosterone. In this study we examined correlations of both testosterone and corticosterone with ectoparasite load and with expression of colorful sexual ornaments (patches on belly and throat) in three species of Sceloporus lizards (S. grammicus, S. megalepidurus, S. torquatus). In addition, we evaluated contributions of sex, body condition, and reproductive season. We expected that individuals with higher testosterone and lower corticosterone levels would have more colorful ornaments than individuals with higher corticosterone levels. In addition, if testosterone has negative effects on immune function but only at higher corticosterone levels, individuals with higher levels of testosterone and corticosterone should have higher ectoparasite loads. Contrary to these expectations, we did not detect an interaction between testosterone and corticosterone statistically affecting either ectoparasite load or the expression of colorful ornaments. Further, we did not find a positive association of either testosterone or corticosterone on ectoparasite loads in any of the three study species. Only in S. grammicus males was a hormone statistically associated with ectoparasite load, but it was a negative association with testosterone. The relationships between both hormones and different aspects of the colorful patches (brightness and chroma) varied drastically among the three species as well as between sexes. Hence, even among congeneric species, we did not observe consistent patterns among color, steroid hormones and ectoparasites. Different associations between these variables may reflect different physiological strategies for the production of colorful signals and immune defense.

Beyond Pairwise Interactions: Multispecies Character Displacement in Mexican Freshwater Fish Communities.

Competition has long been recognized as a central force in shaping evolution, particularly through character displacement. Yet research on character displacement is biased, as it has focused almost exclusively on pairs of interacting species while ignoring multispecies interactions. Communities are seldom so simple that only pairs of species interact, and it is not clear whether inferences from pairwise interactions are sufficient to explain patterns of phenotypes in nature. Here, we test for character displacement in a natural system of freshwater fishes in western Mexico that contains up to four congeneric species of the genus Poeciliopsis. We analyzed body shape differences between populations with different numbers of competitors while accounting for confounding environmental variables. Surprisingly, we found evidence for convergent character displacement in populations of P. prolifica, P. viriosa, and P. latidens. We also found that the convergence in body shape was not consistently in the same direction, meaning that when three or more competitors co-occurred, we did not find more extreme body shapes compared with when there were only two competitors. Instead, when three or more competitors co-occurred, body shape was intermediate between the shape found with a pair of species and the shape found with no competitor present. This intermediate shape suggests that evolution in multispecies communities likely occurs in response to several competitors rather than to simple pairwise interactions. Overall, our results suggest that competition among multiple species is more complex than simple pairwise competitive interactions.

Repeated evolution of viviparity in phrynosomatid lizards constrained interspecific diversification in some life-history traits.

In vertebrates, viviparity has evolved independently multiple times, apparently increasing morphological diversification and speciation rates as a consequence. We tested whether the evolution of viviparity has also increased diversification of life-history traits by estimating evolutionary rates of lizards from the North American family Phrynosomatidae. Using modern phylogenetic comparative methods, we compared these rates between oviparous and viviparous species, and found no support for this hypothesis. Instead, we found higher evolutionary rates for oviparous species in some life-history traits. Our results suggest that the evolution of viviparity may have constrained rather than facilitated evolution of life histories.

Superfetation in live-bearing fishes is not always the result of a morphological constraint.

Superfetation is an unusual reproductive strategy that consists of the presence of multiple broods at different developmental stages within a single female. One hypothesis that was proposed to explain its adaptive significance suggests that, in fishes, superfetation is a response to selective pressures that promote a thin and streamlined body shape, such as high-velocity water systems. Superfetation may allow for reduction in ovary size and hence improve streamlining because superfetating females carry few large, full-term embryos at any given time. We tested this morphological constraint hypothesis using reproductive and morphological data from several populations of two viviparous fishes of the family Poeciliidae (Poeciliopsis gracilis and Poeciliopsis infans). We found no evidence to support the morphological constraint hypothesis. In both species the degree of superfetation varied as a function of a complex interaction between source population and female size, and this interpopulation variation was not associated with the velocity of the water current. Contrary to what we expected, females of P. gracilis with more streamlined bodies were observed in rivers where water velocity is slow or moderate. In P. infans the velocity of the water current did not predict variation in body shape. Our results are noteworthy because a previous study which focused on a congeneric species (Poeciliopsis turrubarensis) demonstrated strong support for this hypothesis. However, based on our evidence we conclude that the association among increased superfetation, streamlined morphologies, and fast-flowing environments is not a general rule and that the adaptive value of superfetation may differ among species.

Evolutionary Interactions Between Visual and Chemical Signals: Chemosignals Compensate for the Loss of a Visual Signal in Male Sceloporus Lizards.

Animals rely on multimodal signals to obtain information from conspecifics through alternative sensory systems, and the evolutionary loss of a signal in one modality may lead to compensation through increased use of signals in an alternative modality. We investigated associations between chemical signaling and evolutionary loss of abdominal color patches in males of four species (two plain-bellied and two colorful-bellied) of Sceloporus lizards. We conducted field trials to compare behavioral responses of male lizards to swabs with femoral gland (FG) secretions from conspecific males and control swabs (clean paper). We also analyzed the volatile organic compound (VOC) composition of male FG secretions by stir bar extraction and gas chromatography-mass spectrometry (GC-MS) to test the hypothesis that loss of the visual signal is associated with elaboration of the chemical signal. Males of plain-bellied, but not colorful-bellied species exhibited different rates of visual displays when exposed to swabs of conspecific FG secretions relative to control swabs. The VOC composition of male Sceloporus FG secretions was similar across all four species, and no clear association between relative abundances of VOCs and evolutionary loss of abdominal color patches was observed. The emerging pattern is that behavioral responses to conspecific chemical signals are species- and context-specific in male Sceloporus, and compensatory changes in receivers, but not signalers may be involved in mediating increased responsiveness to chemical signals in males of plain-bellied species.

Spatial and temporal variation in superfoetation and related life history traits of two viviparous fishes: Poeciliopsis gracilis and P. infans.

Superfoetation is the ability of females to simultaneously bear multiple broods of embryos at different developmental stages. Most studies on the phylogenetic distribution of superfoetation and on the factors that potentially promote superfoetation ignore variation within species. Here, we studied 11 populations of two species of viviparous fishes of the family Poeciliidae (Poeciliopsis gracilis and Poeciliopsis infans) and document wide variation in superfoetation and in three related life history traits: brood size, individual embryo mass and total reproductive allotment. We found significant differences in the average number of simultaneous broods among populations of P. gracilis but not among populations of P. infans. In addition, we found even greater variation between months within populations for both species, although no specific pattern of temporal variation was evident. Instead of the expected consistency of seasonal differences in superfoetation across populations, we found that large variation among months within seasons and the amount and direction of this monthly variation differed widely between populations. Our results emphasize the importance of including intraspecific variation in superfoetation and other life history traits in studies that aimed at finding general explanations of life history trait evolution.

Coping With Urban Habitats Via Glucocorticoid Regulation: Physiology, Behavior, and Life History in Stream Fishes.

As environments become urbanized, tolerant species become more prevalent. The physiological, behavioral and life-history mechanisms associated with the success of such species in urbanized habitats are not well understood, especially in freshwater ecosystems. Here, we examined the glucocorticoid (GC) profiles, life-history traits, and behavior of two species of fish across a gradient of urbanization to understand coping capacity and associated trade-offs. We studied the tolerant live-bearing Western Mosquitofish (Gambusia affinis) for two years and the slightly less tolerant, egg-laying, Blacktail Shiner (Cyprinella venusta) for one year. We used a water-borne hormone method to examine baseline, stress-induced, and recovery cortisol release rates across six streams with differing degrees of urbanization. We also measured life-history traits related to reproduction, and for G. affinis, we measured shoaling behavior and individual activity in a novel arena. Both species showed a trend for reduced stress responsiveness in more urbanized streams, accompanied by higher reproductive output. Although not all populations fit this trend, these results suggest that GC suppression may be adaptive for coping with urban habitats. In G. affinis, GC recovery increased with urbanization, and individuals with the lowest stress response and highest recovery had the greatest reproductive allotment, suggesting that rapid return to baseline GC levels is also an important coping mechanism. In G. affinis, urban populations showed altered life-history trade-offs whereas behavioral traits did not vary systematically with urbanization. Thus, these tolerant species of fish may cope with anthropogenically modified streams by altering their GC profiles and life-history trade-offs. These results contribute to understanding the mechanisms driving species-specific adaptations and thereby community structure in freshwater systems associated with land-use converted areas.

Information out of the blue: phenotypic correlates of abdominal color patches in Sceloporus lizards.

Colorful ornaments are important visual signals for animal communication that can provide critical information about the quality of the signaler. In this study, we focused on different color characteristics of the abdominal patches of males of six lizard species from the genus Sceloporus. We addressed three main objectives. First, we examined if size, brightness, saturation, and conspicuousness of these ornaments are indicative of body size, condition, immune function, or levels of testosterone and corticosterone. Second, we evaluated if the distinct components of these abdominal patches (blue or green patches and black stripes) transmit similar information about the signaler, which would support the redundant signal hypothesis, or if these components are related to different phenotypic traits, which would support the multiple message hypothesis. Third, we compared the phenotypic correlates of these ornaments among our six species to understand the degree of conservatism in the signaling patterns or to find species-specific signals. Using data collected from males in natural conditions and a multi-model inference framework, we found that in most species the area of the patches and the brightness of the blue component are positively related to body size. Thus, these color characteristics are presumably indicative of the physical strength and competitive ability of males and these shared signals were likely inherited from a common ancestor. In half of the species, males in good body condition also exhibit relatively larger blue and black areas, suggesting that the expression of these ornaments is condition-dependent. Abdominal patches also provide information about immunocompetence of the males as indicated by different correlations between certain color characteristics and ectoparasite load, counts of heterophils, and the heterophil:lymphocyte ratio. Our findings reveal that area and brightness of the abdominal patches signal the size and body condition of males, whereas blue saturation and conspicuousness with respect to the surrounding substrate are indicative of immune condition, thus supporting the multiple message hypothesis. However, some of these correlations were not shared by all species and, hence, point to intriguing species-specific signals.

Do ectoparasites affect survival of three species of lizards of the genus Sceloporus?

The short-term effects that ectoparasites cause to their hosts, such as local wounds and secondary infections that occur within a few hours or days after infection, are well documented in a wide variety of taxa, whereas long-term negative effects on the fitness of hosts, which result from chronic infections and are evident after several months, are less understood. Lizards are hosts of distinct species of mites and ticks that cause short-term negative effects such as ulcers, sores and local inflammation. However, the negative effects that these ectoparasites may have on the long-term survival of lizards have not been evaluated. In this study, we collected two years of capture-mark-recapture data and implemented a multi-model inference framework to examine if high ectoparasite loads have negative effects on the long-term survival probability of three lizard species of the genus Sceloporus (S. grammicus, S. megalepidurus, and S. torquatus). In addition, we considered that the potential negative effect of ectoparasites on survival may vary depending on sex, body condition, reproductive season, or climatic season. Contrary to our expectations, our results did not support the hypothesis that high ectoparasite loads reduce the survival probability of these lizards. In S. grammicus and S. megalepidurus we found no evidence of an effect of ectoparasite load on host survival. In S. torquatus ectoparasites influenced survival probability, but the effect was opposite to what we predicted: survival increased substantially as ectoparasite load increased. This unexpected result might be explained by mites discriminating between hosts and attaching more frequently to lizards in better health status, or by high-quality lizards having greater chances of contracting ectoparasites, because these individuals move around large areas and frequently engage in social interactions.

Volatile fatty acid and aldehyde abundances evolve with behavior and habitat temperature in Sceloporus lizards.

Animal signals evolve by striking a balance between the need to convey information through particular habitats and the limitations of what types of signals can most easily be produced and perceived. Here, we present new results from field measures of undisturbed behavior and biochemical analyses of scent marks from 12 species of Sceloporus lizards to explore whether evolutionary changes in chemical composition are better predicted by measures of species behavior, particularly those associated with visual displays, chemoreception, and locomotion, or by measures of habitat climate (precipitation and temperature). We found that more active lizard species used fewer compounds in their volatile scent marks, perhaps conveying less specific information about individual and species identity. Scent marks from more active lizard species also had higher proportions of saturated fatty acids, and the evolution of these compounds has been tracking the phylogeny closely as we would expect for a metabolic byproduct. In contrast, the proportions of unsaturated fatty acids were better explained by evolutionary shifts in habitat temperature (and not precipitation), with species in warmer climates using almost no volatile unsaturated fatty acids. The proportion of aldehydes was explained by both behavior and environment, decreasing with behavioral activity and increasing with habitat temperature. Our results highlight the evolutionary flexibility of complex chemical signals, with different chemical compounds responding to different elements of the selective landscape over evolutionary time.

Differential mortality drives life-history evolution and population dynamics in the fish Brachyrhaphis rhabdophora.

Life-history theory predicts that populations experiencing different levels of extrinsic mortality will evolve divergent reproductive strategies. Previous work in the live-bearing fish Brachyrhaphis rhabdophora shows that individuals from populations that occur with piscivorous fish mature earlier and at smaller sizes and have more and smaller offspring than fish from populations without predators. However, until now, there have been no data to demonstrate that differences in mortality rates actually exist between predator and predator-free sites. Here we present the results of a serial mark-recapture field study designed to estimate mortality rates in natural populations of B. rhabodophora from Costa Rica. We found that fish from predator environments experience higher overall mortality rates and proportionally higher adult mortality rates than fish from predator-free environments. We then ask what impact differences in mortality rates have on B. rhabdophora population dynamics. Using a population matrix modeling approach, we found that B. rhabdophora that co-occur with predators have population growth rates similar to those without predators and both have confidence intervals that span lambda = 1.0. However, elasticity analysis revealed that the most important life-history stages for population growth in predator environments are found early in life and include growth through early ontogenetic stages and survival as small adults; in contrast, the most important life-history stages for population growth in predator-free environments occur late in life, including survival once large juvenile and adult stages are reached. Hence, we demonstrate two important links between predation and population demography, one ecological due to the direct impacts of predator-induced mortality and the other expressed through predator-mediated reproductive adaptation.

Smaller rival males do not affect male mate choice or cortisol but do affect 11-ketotestosterone in a unisexual-bisexual mating complex of fish.

Male mate discrimination may be affected by the social environment (presence or absence of rival males or mates), which can also affect stress and sex hormones (e.g., cortisol and 11-ketotestosterone (11-KT)). The Amazon molly, Poecilia formosa, is an all-female fish species dependent on sperm from mating with male P. latipinna. We investigated male mate choice in P. latipinna between conspecific females and P. formosa with a rival male present and no rival male present. We measured cortisol and 11-KT release rates from all fish. The presence of a rival male had no effect on male mate choice for conspecific females nor overall mating effort. Male 11-KT decreased on the second day after exposure to a rival male on the first day. Focal male 11-KT is positively correlated with the size of the rival male. Both conspecific and heterospecific females released more 11-KT when in the rival male treatment than when not. Neither male nor female cortisol was affected by the presence or absence of the rival male. We did not find an effect of rival males on male mate choice in contrast to our prediction. Instead, our findings may indicate a hormonal response to social competition.

Population dynamics of three lizard species from the genus Sceloporus: short-term changes in demographic parameters.

Most demographic studies focus on numerical changes that occur within populations across years. However, typically studies at an interannual scale do not provide information on the particular times of the year (particular months or seasons) when rates of survival, recruitment, or migration increase or decrease due to physiological, behavioral or ecological processes. These monthly or seasonal changes in demographic parameters may lead to substantial variations in population abundance. In this study, we collected capture-mark-recapture data on 3 species of lizards of the genus Sceloporus (Sceloporus torquatus, Sceloporus grammicus and Sceloporus megalepidurus) found in ecologically similar habitats to examine potential changes in demographic rates among 3 different climatic seasons: rainy, cold-dry and warm-dry seasons. We tested different hypotheses about the effect of these seasons on survival, recruitment of new adults, and temporary emigration. We found that during the season with severe thermal constraints, the cold-dry season, survival of S. torquatus decreased markedly. We also detected a considerable increase in the recruitment rate of S. grammicus during the rainy season, when these lizards are establishing territories and finding mates. In contrast, we found no evidence of intra-annual changes in the rate of temporary emigration. In addition, we calculated abundance and population growth rates for each species and for each season. Our study represents a significant contribution to the understanding of intra-annual demographic variation in lizards.

This town ain't big enough for both of us or is it? Spatial co-occurrence between exotic and native species in an urban reserve.

Exotic species pose a threat to most ecosystems because of their potential to establish negative interactions with native biota. However, exotic species can also offer resources to native species, especially within highly modified environments such as urban ecosystems. We studied 17 exotic-native pairs of species with the potential to compete with one another, or in which one of the species could offer resources to the other, in an urban ecological reserve located within Mexico City. We used two-species occupancy models to analyze the potential association between the presence of the exotic species and the spatial distribution of the native species, as well as to assess if these species tend to avoid each other (negative spatial interaction) or to co-occur more often than expected under the hypothesis of independent occurrences (positive spatial interaction). Our results revealed few cases in which the exotic species influenced occupancy of the native species, and these spatial interactions were mainly positive, indicated by the fact that the occupancy of the native species was usually higher when the exotic species was also present. Seven of the eight observed non-independent patterns of co-occurrence were evident during the dry months of the year, when resources become scarce for most species. Our results also demonstrate that the observed patterns of species co-occurrence depend on the distance to the nearest urban structure and the amount of herb, shrub, and tree cover, indicating that these habitat features influence whether native species avoid or co-occur with exotic species. Our study represents an important contribution to the understanding of temporal dynamics in the co-occurrence between exotic and native species within urban ecological reserves.

Experiencing El Niño conditions during early life reduces recruiting probabilities but not adult survival.

In wild long-lived animals, analysis of impacts of stressful natal conditions on adult performance has rarely embraced the entire age span, and the possibility that costs are expressed late in life has seldom been examined. Using 26 years of data from 8541 fledglings and 1310 adults of the blue-footed booby (Sula nebouxii), a marine bird that can live up to 23 years, we tested whether experiencing the warm waters and food scarcity associated with El Niño in the natal year reduces recruitment or survival over the adult lifetime. Warm water in the natal year reduced the probability of recruiting; each additional degree (°C) of water temperature meant a reduction of roughly 50% in fledglings' probability of returning to the natal colony as breeders. Warm water in the current year impacted adult survival, with greater effect at the oldest ages than during early adulthood. However, warm water in the natal year did not affect survival at any age over the adult lifespan. A previous study showed that early recruitment and widely spaced breeding allow boobies that experience warm waters in the natal year to achieve normal fledgling production over the first 10 years; our results now show that this reproductive effort incurs no survival penalty, not even late in life. This pattern is additional evidence of buffering against stressful natal conditions via life-history adjustments.

Morphological structures for potential sperm storage in poeciliid fishes. Does superfetation matter?

Sperm storage within the female reproductive tract has been reported as a reproductive strategy in several species of vertebrates and invertebrates. However, the morphological structures that allow for sperm to be stored and kept viable for long periods are relatively unknown in osteichthyes. We use histological and stereological tools to identify and quantify sperm storage structures (spermathecae) in 12 species of viviparous Poeciliidae. We found spermathecae in nine species, six of which exhibit superfetation (the ability of females to simultaneously carry within the ovary two or more broods of embryos at different stages of development). These spermathecae are folds of ovarian tissue that close around spermatozoa. We compared the number and size (volume) of spermathecae between species with and without superfetation. Species that exhibit superfetation had a significantly higher number of spermathecae than species that do not exhibit this reproductive strategy. In addition, we found that the mean volume of spermathecae and total volume of spermathecae present in the ovary are marginally higher in species with superfetation. Our results contribute to the understanding of the morphological structures that allow for sperm storage in viviparous osteichthyes and suggest a positive relationship between superfetation and the capacity of females to store sperm.

Shaping communicative colour signals over evolutionary time.

Many evolutionary forces can shape the evolution of communicative signals, and the long-term impact of each force may depend on relative timing and magnitude. We use a phylogenetic analysis to infer the history of blue belly patches of Sceloporus lizards, and a detailed spectrophotometric analysis of four species to explore the specific forces shaping evolutionary change. We find that the ancestor of Sceloporus had blue patches. We then focus on four species; the first evolutionary shift (captured by comparison of S. merriami and S. siniferus) represents an ancient loss of the belly patch by S. siniferus, and the second evolutionary shift, bounded by S. undulatus and S. virgatus, represents a more recent loss of blue belly patch by S. virgatus. Conspicuousness measurements suggest that the species with the recent loss (S. virgatus) is the least conspicuous. Results for two other species (S. siniferus and S. merriami) suggest that over longer periods of evolutionary time, new signal colours have arisen which minimize absolute contrast with the habitat while maximizing conspicuousness to a lizard receiver. Specifically, males of the species representing an ancient loss of blue patch (S. siniferus) are more conspicuous than are females in the UV, whereas S. merriami males have evolved a green element that makes their belly patches highly sexually dimorphic but no more conspicuous than the white bellies of S. merriami females. Thus, our results suggest that natural selection may act more immediately to reduce conspicuousness, whereas sexual selection may have a more complex impact on communicative signals through the introduction of new colours.