Bacteria in the Reproductive Tracts of Red-Winged Blackbirds

Abstract

We identified bacteria collected from the ejaculates and cloacae of male Red-winged Blackbirds (Agelaius phoeniceus) and from the cloacae of their mates during two breeding seasons and at three geographic locations with two distinct breeding habitats in each. In all, 42% of 233 ejaculates contained at least one bacteria species. Analysis of control samples suggested that some bacteria come from contamination during collection, but most are either carried within the ejaculate or are present on the male cloaca. As in an earlier study of Agelaius phoeniceus, we recorded many different species with considerable diversity between samples. We tested several explanations for this diversity. We found no overlap in either the presence of bacteria or the species found in multiple ejaculates obtained from the same male. We also found no association between bacteria in the ejaculate and those in the cloaca from the same male, or in samples collected from a male and those from the females nesting on his territory. Surveys of ejaculates from three locations, Kentucky, New York, and Wisconsin, yielded similar patterns of prevalence and diversity. Ejaculate samples from males inhabiting relatively dry upland habitats contained a similar number of bacteria and array of species as males inhabiting relatively wet, marshy territories. Many of the isolated bacteria are probably benign, but pathological effects of some species have been recorded in some circumstances. Our results suggest that acquiring pathogenic bacteria represents a potential cost to multiple mating by females, but the potential benefits of some microbes may offset these risks. Bacterias en el Sistema Reproductivo de Agelaius phoeniceus Resumen. Identificamos bacterias aisladas del semen eyaculado y de las cloacas de machos de la especie Agelaius phoeniceus y de las cloacas de sus parejas hembras durante dos estaciones y en tres áreas geográficas, con dos tipos de hábitat en cada área. En general, el 42% de las 233 muestras de eyaculaciones presentó por lo menos una especie de bacteria. El análisis de las muestras control sugiere que algunas bacterias provienen de contaminación ambiental durante la colecta, pero la mayoría de las bacterias provienen del semen o están presentes en la cloaca del macho. Al igual que en un estudio anterior con Agelaius phoeniceus, registramos muchas especies distintas, con bastante diversidad entre las muestras. Pusimos a prueba algunas hipótesis que podrían explicar esta diversidad. No encontramos coincidencia ni en la presencia de bacterias ni en las especies encontradas entre múltiples muestras obtenidas de un mismo macho. Tampoco encontramos correspondencia entre las bacterias presentes en las muestras de semen y de la cloaca de un mismo macho, ni entre las muestras colectadas de los machos y de las hembras que se encuentran anidando en su territorio. El estudio de muestras de eyaculaciones provenientes de tres localidades, Kentucky, New York, y Wisconsin, produjo patrones similares de prevalencia y diversidad. Muestras de semen de machos que habitan ambientes relativamente secos en tierras altas presentaron números de bacterias y especies similares a las muestras colectadas de machos que habitan territorios pantanosos. Probablemente, muchas de las bacterias son benignas, pero en ciertas circunstancias se han registrado efectos patológicos de algunas especies. Nuestros resultados sugieren que adquirir bacterias patológicas es un posible costo del apareamiento múltiple de las hembras, pero los posibles beneficios de algunos microbios podrían compensar estos riesgos.

Testosterone levels are positively correlated with cloacal bacterial diversity and the relative abundance of Chlamydiae in breeding male rufous‐collared sparrows

“…During copulation in birds, even if there is no intromission, there is cloacal contact which allows bacterial transmission between individuals (Westneat & Rambo ; Hupton et al . ; Kulkarni & Heeb ). Having multiple partners has the potential to result in increased exposure to different cloacal bacteria.…”

Promiscuity in mice is associated with increased vaginal bacterial diversity

“…and opportunistic pathogens (e.g., many Pseudomonas spp .) have been described in the lower reproductive tract of females of multiple species including humans (Kim et al 2009; Witkin et al 2007; Brown et al 2007), red-winged blackbirds (Hupton et al 2003), and the koala (Weigler et al 1988). Although explicit tests of the host fitness consequences of these infections are generally lacking, given that bacterial infections have been shown to be able to influence host phenotype (Brook 2005; Servin 2004), we might expect to see fitness effects associated with the bacterial colonization of reproductive structures.…”

Genitalia‐associated microbes in insects

“…Only few reports exist on the presence of opportunistic microbes within or on reproductive organs in insects (Reinhardt et al ., ; Otti et al ., ; Rizzi et al ., ) and to my knowledge no study has so far addressed the direct effect of opportunistic microbes on reproduction via sexual transmission (see also Table ). In vertebrates, including humans, microbes are present on male reproductive organs as well as in semen (Lombardo & Thorpe, ; Hupton et al ., ; Skau & Folstad, ; Virecoulon et al ., ; González‐Marín et al ., ). The female genitals also harbor a rich microbial flora in birds and mammals, again including humans (Hirsh, ; Hupton et al ., ; White et al ., ).…”

“…In vertebrates, including humans, microbes are present on male reproductive organs as well as in semen (Lombardo & Thorpe, ; Hupton et al ., ; Skau & Folstad, ; Virecoulon et al ., ; González‐Marín et al ., ). The female genitals also harbor a rich microbial flora in birds and mammals, again including humans (Hirsh, ; Hupton et al ., ; White et al ., ). For example, in primates those genital microbiomes vary between species (Stumpf et al ., ) and are, at least in humans, sexually dimorphic (Cho & Blaser, ; Human Microbiome Project Consortium, ).…”