Sam Diaz-Munoz | New York University (original) (raw)

Papers by Sam Diaz-Munoz

Advances in Applied Microbiology, 2014

Phages are considered the most abundant and diverse biological entities on Earth and are notable ... more Phages are considered the most abundant and diverse biological entities on Earth and are notable not only for their sheer abundance, but also for their influence on bacterial hosts. In nature, bacteria–phage relationships are complex and have far-reaching consequences beyond particular pairwise interactions, influencing everything from bacterial virulence to eukaryotic fitness to the carbon cycle. In this review, we examine bacteria and phage distributions in nature first by highlighting biogeographic patterns and nonhost environmental influences on phage distribution, then by considering the ways in which phages and bacteria interact, emphasizing phage life cycles, bacterial responses to phage infection, and the complex patterns of phage host specificity. Finally, we discuss phage impacts on bacterial abundance, genetics, and physiology, and further aim to clarify distinctions between current theoretical models and point out areas in need of future research.

BMC Evolutionary Biology, 2013

Background: Sex presents evolutionary costs and benefits, leading to the expectation that the amo... more Background: Sex presents evolutionary costs and benefits, leading to the expectation that the amount of genetic exchange should vary in conditions with contrasting cost-benefit equations. Like eukaryotes, viruses also engage in sex, but the rate of genetic exchange is often assumed to be a relatively invariant property of a particular virus. However, the rates of genetic exchange can vary within one type of virus according to geography, as highlighted by phylogeographic studies of cystoviruses. Here we merge environmental microbiology with experimental evolution to examine sex in a diverse set of cystoviruses, consisting of the bacteriophage φ6 and its relatives.
To quantify reassortment we manipulated – by experimental evolution – electrophoretic mobility of intact virus particles for use as a phenotypic marker to estimate genetic exchange.

Results: We generated descendants of φ6 that exhibited fast and slow mobility during gel electrophoresis. We identified mutations associated with slow and fast phenotypes using whole genome sequencing and used crosses to establish the production of hybrids of intermediate mobility. We documented natural variation in electrophoretic mobility among environmental isolates of cystoviruses and used crosses against a common fast mobility φ6 strain to monitor the production of hybrids with intermediate mobility, thus estimating the amount of genetic exchange. Cystoviruses from different geographic locations have very different reassortment rates when measured against φ6, with viruses isolated from California showing higher reassortment rates than those from the Northeastern US.

Conclusions: The results confirm that cystoviruses from different geographic locations have remarkably different reassortment rates –despite similar genome structure and replication mechanisms– and that these differences are in large part due to sexual reproduction. This suggests that particular viruses may indeed exhibit diverse sexual behavior, but wide geographic sampling, across varying environmental conditions may be necessary to characterize the full repertoire. Variation in reassortment rates can assist in the delineation of viral populations and is likely to provide insight into important viral evolutionary dynamics including the rate of coinfection, virulence, and host range shifts. Electrophoretic mobility may be an indicator of important determinants of fitness and the techniques herein can be applied to the study of other viruses.

Male reproductive cooperation is rare in nature: expectations from evolutionary theory suggest th... more Male reproductive cooperation is rare in nature: expectations from evolutionary theory suggest that males should be competitors for reproductive opportunities and provide little parental care. Counter to this expectation, in cooperatively polyandrous mating systems, multiple adult males mate with a single breeding female and subsequently cooperate to rear her young. This raises the question of the fitness benefits of parental care, as males may be providing care to offspring that are not their own. Here, I use genetic and demographic data from a multiyear field study of Geoffroy’s tamarin, Saguinus geoffroyi, to test predictions of the indirect and direct fitness benefits hypotheses. I found that polyandrous males within a group were related at levels consistent with filial or fraternal relationships (r = 0.36–0.44) and could also share paternity (40% of groups had >2 male sires). Sharing of paternity occurred both within litters and over multiyear associations that remained stable throughout the study period of 2–3 years. However, remaining groups had a single sire, perhaps owing to the ability of males to prevail in sperm competition. These results suggest the joint role of indirect and direct fitness benefits in male–male cooperation in tamarins, in contrast to other cooperatively polyandrous species. The high average relatedness of polyandrous males may be consistent with fraternal cooperative polyandry in this species, as observed in certain human societies, providing a novel example that should enhance comparative studies of the evolution of male–male cooperation in reproduction.

PeerJ 2:e640, 2014

An influential hypothesis proposed by Greenwood (1980) suggests that different mating systems res... more An influential hypothesis proposed by Greenwood (1980) suggests that different mating systems result in female and male-biased dispersal, respectively, in birds and mammals. However, other aspects of social structure and behavior can also shape sex-biased dispersal. Although sex-specific patterns of kin cooperation are expected to affect the benefits of philopatry and dispersal patterns, empirical evidence is scarce. Unlike many mammals, Saguinus geoffroyi (Geoffroy’s tamarin) has a breeding system in which typically multiple males mate with a single breeding female. Males typically form cooperative reproductive partnerships between relatives, whereas females generally compete for reproductive opportunities. This system of cooperative polyandry is predicted to result in female-biased dispersal, providing an opportunity to test the current hypotheses of sex-biased dispersal. Here we test for evidence of sex-biased dispersal in S. geoffroyi using demographic and genetic data from three populations. We find no sex bias in natal dispersal, contrary to the prediction based on the mating patterns. This pattern was consistent after controlling for the effects of historical population structure. Limited breeding opportunities within social groups likely drive both males and females to disperse, suggesting that dispersal is intimately related to the social context. The integration of genetic and field data revealed that tamarins are another exception to the presumed pattern of male-biased dispersal
in mammals. A shift in focus from mating systems to social behavior, which plays a role in most all processes expected to influence sex-bias in dispersal, will be a fruitful target for research both within species and across taxa.

The role of physical barriers in promoting population divergence and genetic structuring is well ... more The role of physical barriers in promoting population divergence and genetic structuring is well known. While it is well established that animals can show genetic structuring at small spatial scales, less well-resolved is how the timing of the appearance of barriers affects population structure. This study uses the Panama Canal watershed as a test of the effects of old and recent riverine barriers in creating population structure in Saguinus geoffroyi, a small cooperatively breeding Neotropical primate. Mitochondrial sequences and microsatellite genotypes from three sampling localities revealed genetic structure across the Chagres River and the Panama Canal, suggesting that both waterways act as barriers to gene flow. F-statistics and exact tests of population differentiation suggest population structure on either side of both riverine barriers. Genetic differentiation across the Canal, however, was less than observed across the Chagres. Accordingly, Bayesian clustering algorithms detected between two and three populations, with localities across the older Chagres River always assigned as distinct populations. While conclusions represent a preliminary assessment of genetic structure of S. geoffroyi, this study adds to the evidence indicating that riverine barriers create genetic structure across a wide variety of taxa in the Panama Canal watershed and highlights the potential of this study area for discerning modern from historical influences on observed patterns of population genetic structure.

Genes, Brain and …

Discoveries of how social behavior can influence the plasticity of gonadotropin-releasing hormone... more Discoveries of how social behavior can influence the plasticity of gonadotropin-releasing hormone (GnRH) have revolutionized the field of behavioral neuroendocrinology by providing new insights into the neural mechanisms controlling behavior. In 2000, the neuropeptide gonadotropin inhibitory hormone (GnIH) was discovered and is changing the way we view how the brain mediates reproduction and associated behaviors. GnIH acts as a reproductive ‘pause button’, momentarily inhibiting the activity of the reproductive system. However, how GnIH fluctuates naturally in response to social environment is unknown. We examine how the outcome of competition for limited resources needed for reproduction is associated with GnIH. We experimentally manipulated nesting opportunities for pairs of European starlings (Sturnus vulgaris) and examined brain GnIH mRNA and peptide content, as well as GnRH content and plasma testosterone and corticosterone. By limiting the number of nest boxes per enclosure and thus the number of social pairing and nesting opportunities, we observed that birds which outcompeted others for nest boxes (‘winners’) had significantly fewer numbers of GnIH peptide-producing cells than those without nest boxes (‘losers’) and this relationship changed with breeding stage. GnRH content, testosterone and corticosterone did not vary with nest box ownership. Thus, while birds appeared reproductively capable across treatments, our data indicate that GnIH may serve as a modulator of reproductive behaviors in response to social environment. Additionally, we provide some evidence of the adaptive value of this mechanism.

Advances in Applied Microbiology, 2014

Phages are considered the most abundant and diverse biological entities on Earth and are notable ... more Phages are considered the most abundant and diverse biological entities on Earth and are notable not only for their sheer abundance, but also for their influence on bacterial hosts. In nature, bacteria–phage relationships are complex and have far-reaching consequences beyond particular pairwise interactions, influencing everything from bacterial virulence to eukaryotic fitness to the carbon cycle. In this review, we examine bacteria and phage distributions in nature first by highlighting biogeographic patterns and nonhost environmental influences on phage distribution, then by considering the ways in which phages and bacteria interact, emphasizing phage life cycles, bacterial responses to phage infection, and the complex patterns of phage host specificity. Finally, we discuss phage impacts on bacterial abundance, genetics, and physiology, and further aim to clarify distinctions between current theoretical models and point out areas in need of future research.

BMC Evolutionary Biology, 2013

Background: Sex presents evolutionary costs and benefits, leading to the expectation that the amo... more Background: Sex presents evolutionary costs and benefits, leading to the expectation that the amount of genetic exchange should vary in conditions with contrasting cost-benefit equations. Like eukaryotes, viruses also engage in sex, but the rate of genetic exchange is often assumed to be a relatively invariant property of a particular virus. However, the rates of genetic exchange can vary within one type of virus according to geography, as highlighted by phylogeographic studies of cystoviruses. Here we merge environmental microbiology with experimental evolution to examine sex in a diverse set of cystoviruses, consisting of the bacteriophage φ6 and its relatives.
To quantify reassortment we manipulated – by experimental evolution – electrophoretic mobility of intact virus particles for use as a phenotypic marker to estimate genetic exchange.

Results: We generated descendants of φ6 that exhibited fast and slow mobility during gel electrophoresis. We identified mutations associated with slow and fast phenotypes using whole genome sequencing and used crosses to establish the production of hybrids of intermediate mobility. We documented natural variation in electrophoretic mobility among environmental isolates of cystoviruses and used crosses against a common fast mobility φ6 strain to monitor the production of hybrids with intermediate mobility, thus estimating the amount of genetic exchange. Cystoviruses from different geographic locations have very different reassortment rates when measured against φ6, with viruses isolated from California showing higher reassortment rates than those from the Northeastern US.

Conclusions: The results confirm that cystoviruses from different geographic locations have remarkably different reassortment rates –despite similar genome structure and replication mechanisms– and that these differences are in large part due to sexual reproduction. This suggests that particular viruses may indeed exhibit diverse sexual behavior, but wide geographic sampling, across varying environmental conditions may be necessary to characterize the full repertoire. Variation in reassortment rates can assist in the delineation of viral populations and is likely to provide insight into important viral evolutionary dynamics including the rate of coinfection, virulence, and host range shifts. Electrophoretic mobility may be an indicator of important determinants of fitness and the techniques herein can be applied to the study of other viruses.

Male reproductive cooperation is rare in nature: expectations from evolutionary theory suggest th... more Male reproductive cooperation is rare in nature: expectations from evolutionary theory suggest that males should be competitors for reproductive opportunities and provide little parental care. Counter to this expectation, in cooperatively polyandrous mating systems, multiple adult males mate with a single breeding female and subsequently cooperate to rear her young. This raises the question of the fitness benefits of parental care, as males may be providing care to offspring that are not their own. Here, I use genetic and demographic data from a multiyear field study of Geoffroy’s tamarin, Saguinus geoffroyi, to test predictions of the indirect and direct fitness benefits hypotheses. I found that polyandrous males within a group were related at levels consistent with filial or fraternal relationships (r = 0.36–0.44) and could also share paternity (40% of groups had >2 male sires). Sharing of paternity occurred both within litters and over multiyear associations that remained stable throughout the study period of 2–3 years. However, remaining groups had a single sire, perhaps owing to the ability of males to prevail in sperm competition. These results suggest the joint role of indirect and direct fitness benefits in male–male cooperation in tamarins, in contrast to other cooperatively polyandrous species. The high average relatedness of polyandrous males may be consistent with fraternal cooperative polyandry in this species, as observed in certain human societies, providing a novel example that should enhance comparative studies of the evolution of male–male cooperation in reproduction.

PeerJ 2:e640, 2014

An influential hypothesis proposed by Greenwood (1980) suggests that different mating systems res... more An influential hypothesis proposed by Greenwood (1980) suggests that different mating systems result in female and male-biased dispersal, respectively, in birds and mammals. However, other aspects of social structure and behavior can also shape sex-biased dispersal. Although sex-specific patterns of kin cooperation are expected to affect the benefits of philopatry and dispersal patterns, empirical evidence is scarce. Unlike many mammals, Saguinus geoffroyi (Geoffroy’s tamarin) has a breeding system in which typically multiple males mate with a single breeding female. Males typically form cooperative reproductive partnerships between relatives, whereas females generally compete for reproductive opportunities. This system of cooperative polyandry is predicted to result in female-biased dispersal, providing an opportunity to test the current hypotheses of sex-biased dispersal. Here we test for evidence of sex-biased dispersal in S. geoffroyi using demographic and genetic data from three populations. We find no sex bias in natal dispersal, contrary to the prediction based on the mating patterns. This pattern was consistent after controlling for the effects of historical population structure. Limited breeding opportunities within social groups likely drive both males and females to disperse, suggesting that dispersal is intimately related to the social context. The integration of genetic and field data revealed that tamarins are another exception to the presumed pattern of male-biased dispersal
in mammals. A shift in focus from mating systems to social behavior, which plays a role in most all processes expected to influence sex-bias in dispersal, will be a fruitful target for research both within species and across taxa.

The role of physical barriers in promoting population divergence and genetic structuring is well ... more The role of physical barriers in promoting population divergence and genetic structuring is well known. While it is well established that animals can show genetic structuring at small spatial scales, less well-resolved is how the timing of the appearance of barriers affects population structure. This study uses the Panama Canal watershed as a test of the effects of old and recent riverine barriers in creating population structure in Saguinus geoffroyi, a small cooperatively breeding Neotropical primate. Mitochondrial sequences and microsatellite genotypes from three sampling localities revealed genetic structure across the Chagres River and the Panama Canal, suggesting that both waterways act as barriers to gene flow. F-statistics and exact tests of population differentiation suggest population structure on either side of both riverine barriers. Genetic differentiation across the Canal, however, was less than observed across the Chagres. Accordingly, Bayesian clustering algorithms detected between two and three populations, with localities across the older Chagres River always assigned as distinct populations. While conclusions represent a preliminary assessment of genetic structure of S. geoffroyi, this study adds to the evidence indicating that riverine barriers create genetic structure across a wide variety of taxa in the Panama Canal watershed and highlights the potential of this study area for discerning modern from historical influences on observed patterns of population genetic structure.

Genes, Brain and …

Discoveries of how social behavior can influence the plasticity of gonadotropin-releasing hormone... more Discoveries of how social behavior can influence the plasticity of gonadotropin-releasing hormone (GnRH) have revolutionized the field of behavioral neuroendocrinology by providing new insights into the neural mechanisms controlling behavior. In 2000, the neuropeptide gonadotropin inhibitory hormone (GnIH) was discovered and is changing the way we view how the brain mediates reproduction and associated behaviors. GnIH acts as a reproductive ‘pause button’, momentarily inhibiting the activity of the reproductive system. However, how GnIH fluctuates naturally in response to social environment is unknown. We examine how the outcome of competition for limited resources needed for reproduction is associated with GnIH. We experimentally manipulated nesting opportunities for pairs of European starlings (Sturnus vulgaris) and examined brain GnIH mRNA and peptide content, as well as GnRH content and plasma testosterone and corticosterone. By limiting the number of nest boxes per enclosure and thus the number of social pairing and nesting opportunities, we observed that birds which outcompeted others for nest boxes (‘winners’) had significantly fewer numbers of GnIH peptide-producing cells than those without nest boxes (‘losers’) and this relationship changed with breeding stage. GnRH content, testosterone and corticosterone did not vary with nest box ownership. Thus, while birds appeared reproductively capable across treatments, our data indicate that GnIH may serve as a modulator of reproductive behaviors in response to social environment. Additionally, we provide some evidence of the adaptive value of this mechanism.