Molecular biogeography and host relations of a parasitoid fly

© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Successful geographic range expansion by parasites and parasitoids may also require host range expansion. Thus, the evolutionary advantages of host specialization may trade off against the ability to exploit new host species encountered in new geographic regions. Here, we use molecular techniques and confirmed host records to examine biogeography, population divergence, and host flexibility of the parasitoid fly, Ormia ochracea (Bigot). Gravid females of this fly find their cricket hosts acoustically by eavesdropping on male cricket calling songs; these songs vary greatly among the known host species of crickets. Using both nuclear and mitochondrial genetic markers, we (a) describe the geographical distribution and subdivision of genetic variation in O. ochracea from across the continental United States, the Mexican states of Sonora and Oaxaca, and populations introduced to Hawaii; (b) demonstrate that the distribution of genetic variation among fly populations is consistent with a single widespread species with regional host specialization, rather than locally differentiated cryptic species; (c) identify the more-probable source populations for the flies introduced to the Hawaiian islands; (d) examine genetic variation and substructure within Hawaii; (e) show that among-population geographic, genetic, and host song distances are all correlated; and (f) discuss specialization and lability in host-finding behavior in light of the diversity of cricket songs serving as host cues in different geographically separate populations

Innate Immunity and the Evolution of Resistance to an Emerging Infectious Disease in a Wild Bird

Innate immunity is expected to play a primary role in conferring resistance to novel infectious diseases, but few studies have attempted to examine its role in the evolution of resistance to emerging pathogens in wild vertebrate populations. Here, we used experimental infections and cDNA microarrays to examine whether changes in the innate and/or acquired immune responses likely accompanied the emergence of resistance in house finches (Carpodacus mexicanus) in the eastern United States subject to a recent outbreak of conjunctivitis-causing bacterium (Mycoplasma gallisepticum—MG). Three days following experimental infection with MG, we observed differences in the splenic transcriptional responses between house finches from eastern U.S. populations, with a 12-year history of MG exposure, versus western U.S. populations, with no history of exposure to MG. In particular, western birds down-regulated gene expression, while eastern finches showed no expression change relative to controls. Studies involving poultry have shown that MG can manipulate host immunity, and our observations suggest that pathogen manipulation occurred only in finches from the western populations, outside the range of MG. Fourteen days after infection, eastern finches, but not western finches, up-regulated genes associated with acquired immunity (cell-mediated immunity) relative to controls. These observations suggest population differences in the temporal course of the response to infection with MG and imply that innate immune processes were targets of selection in response to MG in the eastern U.S. population.Organismic and Evolutionary Biolog

Ultrafast Evolution and Loss of CRISPRs Following a Host Shift in a Novel Wildlife Pathogen, Mycoplasma gallisepticum

Measureable rates of genome evolution are well documented in human pathogens but are less well understood in bacterial pathogens in the wild, particularly during and after host switches. Mycoplasma gallisepticum (MG) is a pathogenic bacterium that has evolved predominantly in poultry and recently jumped to wild house finches (Carpodacus mexicanus), a common North American songbird. For the first time we characterize the genome and measure rates of genome evolution in House Finch isolates of MG, as well as in poultry outgroups. Using whole-genome sequences of 12 House Finch isolates across a 13-year serial sample and an additional four newly sequenced poultry strains, we estimate a nucleotide diversity in House Finch isolates of only ∼2% of ancestral poultry strains and a nucleotide substitution rate of 0.8−1.2×10−5 per site per year both in poultry and in House Finches, an exceptionally fast rate rivaling some of the highest estimates reported thus far for bacteria. We also found high diversity and complete turnover of CRISPR arrays in poultry MG strains prior to the switch to the House Finch host, but after the invasion of House Finches there is progressive loss of CRISPR repeat diversity, and recruitment of novel CRISPR repeats ceases. Recent (2007) House Finch MG strains retain only ∼50% of the CRISPR repertoire founding (1994–95) strains and have lost the CRISPR–associated genes required for CRISPR function. Our results suggest that genome evolution in bacterial pathogens of wild birds can be extremely rapid and in this case is accompanied by apparent functional loss of CRISPRs

Data from: Roaming Romeos: male crickets evolving in silence show increased locomotor behaviours

Loss of sexual signals should be strongly selected against when these signals are necessary for mate attraction or acquisition. Male Teleogryllus oceanicus field crickets produce a long-distance calling song to attract females. Separate genetic mutations recently evolved on the Hawaiian Islands of Kauai and Oahu, rendering approximately 90% and 50% of males, respectively, incapable of calling. We examined whether males from three populations, each with a distinct prevalence of this silent ‘flatwing’ phenotype, show behavioural plasticity in response to being reared in a call-less environment. Crickets from Kauai, Oahu and Mangaia, a Cook Islands population without the flatwing phenotype, either were or were not exposed to calling song during late juvenile and early adult development. Movement assays showed that when males originating from Kauai were reared in silence, they moved sooner, moved more and spent more time walking during silent behaviour trials than did their counterparts reared with calling song. Males from Oahu and Mangaia, however, showed no such effect of acoustic rearing environment on these behaviours. This suggests that there has been directional selection on Kauai for males to respond to a silent environment by increasing their mobility, thus compensating for their lack of song and increasing their chance of encountering receptive females

Balenger_DataDryad

File contains movement behavior data and morphological data (size and wing morph) for each individual used in this study

Balenger_cricket_density_data

Balenger_cricket_density_dat

Data from: Is it the song or the singers? Acoustic and social experiences shape adult reproductive tactics and condition

When sexual signals are perceived during growth and development they can provide information regarding the social conditions likely to be encountered as an adult. Perception of cues related to the presence and density of future mates and potential competitors can result in altered adult phenotypes. Previous studies have shown that adult male Teleogryllus oceanicus field crickets from a Kauai, Hawaii population reared alone and without hearing conspecific song are more phonotactic than those reared with song. These naïve males also reduce investment in body size and immunity. Here we examined whether another source of population density information, the presence of other males, affects behavior, size, and immunity. Specifically, we examined satellite behavior as evidenced by strength of phonotaxis, body condition, and immune response in males reared singly and in groups in the presence and absence of conspecific song. Body condition did not vary with rearing density, and immune response did not vary with either acoustic environment or rearing density. Interestingly, group-housed males were more phonotactic than singly-housed males. This pattern was largely driven by the low levels of phonotaxis exhibited by males that were singly-housed in the presence of conspecific song. These findings suggest that males respond to social cues in addition to conspecific song, but that these cues do not necessarily provide concordant information

Sexual selection in a socially monogamous bird: male color predicts paternity success in the mountain bluebird, Sialia currucoides. Behavioral Ecology and Sociobiology

Abstract Ornamental traits are thought to evolve because they give individuals an advantage in securing multiple mates. Thus, the presence of ornamentation among males in many monogamous bird species presents something of a conundrum. Under certain conditions, extra-pair paternity can increase the variance in reproductive success among males, thus increasing the potential for sexual selection to act. We addressed this possibility in the mountain bluebird (Sialia currucoides), a socially monogamous songbird in which males possess brilliant ultraviolet (UV)-blue plumage. Specifically, we asked whether a male's success at siring offspring within his own nest and within the nests of other males was related to his coloration. In pairwise comparisons, males that sired extra-pair offspring were not more colorful than the males that they cuckolded. However, males that sired at least one extra-pair offspring were, on average, brighter and more UV-blue than males that did not sire extra-pair offspring. Brighter, more UV-blue males sired more offspring both with their own mate and tended to sire more offspring with extra-pair mates and thus sired more offspring overall. Our results support the hypothesis that the brilliant UV-blue ornamental plumage of male mountain bluebirds evolved at least in part because it provides males with an advantage in fertilizing the eggs of multiple females

Data for Heinen-Kay et al. Sexual signal loss and female reproduction

Data for (1) comparison of flatwing and normal-wing homozygous female reproductive tissue, (2) offspring production of flatwing and normal-wing females, and (3) reproductive tissue comparison between populations and acoustic treatment