Co-opting responses for old enemies

On Friday, Shelby Gantt introduced us to an unusual type of parasite, the brood parasite! As Shelby eloquently described, brood parasitism is when an individual’s offspring are raised by someone else who incurs a cost to raising these offspring. The most well-known examples of bird brood parasitism are the cuckoo and the cowbird, but at least 100 species of birds (nearly 1% of all bird species) are obligate parasites on the nests of at least 950 or >10% other species of birds (Abolins-Abols & Hauber 2018). The costs to the foster parents include a reduction in the size and fledging success of the foster parents’ biological offspring and a potential decrease in future reproductive success due to the energetic costs of feeding the foster chick.

These parasitized species have evolved a variety of defenses against brood parasitism, including chasing off the brood parasite before an egg is laid, abandoning a nest with a parasitic egg or ejecting the egg from the nest, or reducing care to the parasitic nestling (Abolins-Abols & Hauber 2018). Some of these strategies may have been co-opted from behavioral and physiological responses to conspecific competitors. For example, the behaviors involved in defending one’s territory from a rival male, e.g., vigilance and attacking, are similar to the behaviors involved in driving away a brood parasite. But are the underlying physiological and genomic mechanisms the same?

The red-winged blackbird (Agelaius phoeniceus; hereafter redwings) is an abundant North American songbird whose nests are frequently parasitized (~17% of nests) by the brown-headed cowbird (Molothrus ater; Clotfelter & Yasukawa 1999). By nesting in large groups, redwings protect their nests from predation and parasitism through group vigilance and by aggressively driving away female cowbirds before they have an opportunity to lay an egg (Clotfelter 1997; Yasukawa et al. 2016). Male redwings also respond strongly to intruder male redwings by intense singing and displaying their red epaulets followed by chasing and attacking a persistent intruder (Peek 1972; see the redwing male vocal & visual territorial display here). However, male redwings do not respond strongly to non-parasitic species.

Louder et al. (2020) played the songs of three ‘intruders’ to wild, free-living male redwings while they were on their breeding season territories: unfamiliar conspecifics (male redwings), parasitic heterospecific (female cowbird chatters), and control heterospecific vocalizations (dove coos). Follow these links to learn more about these birds and click on the Listen button to hear their calls: Redwings, cowbirds, and doves. Each male heard one type of song during these ‘playback’ experiments, and their behavioral responses were recorded. Then the males were caught via mist-nets, and the authors collected blood samples, which were then assessed for gene expression using RNAseq to see if the proximate physiological and transcriptomic mechanisms activated by rival male redwings or parasitic female cowbirds were similar.

Behaviorally, male redwings sang significantly more in response to rival redwing males, but approached rival males and parasitic female cowbirds in equal frequencies. Transcriptomically, the authors did not find significant patterns of differential gene expression in response to the different playback conditions either in overall gene expression or in 20 candidate biomarker genes. However, when they looked for gene networks where the expression of many genes differed in the same direction, an analysis called a weighted gene co-expression network analysis (WGCNA; Langfelder & Horvath 2008), they found that genes involved in metabolism and gene regulation were up-regulated in response to conspecific males. Interestingly, in response to the songs of both rival male redwings and parasitic cowbird females, genes involved in immune response like virus and cytokine-mediated pathways were down-regulated. In other words, the response to male rivals differed from the response to heterospecific birds (either parasites or harmless doves) in terms of singing and up-regulation of genes involved in metabolism. But male redwings responded similarly to male rivals and female parasites in terms of number and proximity of approaches as well as down-regulation of genes involved in immune function. The fact that the down-regulated genes are involved in the immune response may indicate a trade-off between aggressive behavior and immune function (a common trade-off in other vertebrates) since energy resources are limited. Ultimately, the aggressive response to brood parasites can involve similar transcriptomic and physiological responses as the response to a rival conspecific, suggesting there may be shared pathways engaged in recognition and reaction to ‘old and new enemies’.

References:

Abolins-Abols, M., & Hauber, M. E. (2018). Host defences against avian brood parasitism: an endocrine perspective. Proceedings of the Royal Society B: Biological Sciences, 285(1886), 20180980. https://doi.org/10.1098/rspb.2018.0980

Clotfelter, E. (1997). Red-Winged Blackbird Parental Investment following Brood Parasitism by Brown-Headed Cowbirds: Is Parentage Important? Behavioral Ecology and Sociobiology, 41(3), 193-201. https://doi.org/10.1007/s002650050379

Clotfelter, E., & Yasukawa, K. (1999). The Effect of Aggregated Nesting on Red-Winged Blackbird Nest Success and Brood Parasitism by Brown-Headed Cowbirds. The Condor, 101(4), 729-736. https://doi.org/10.2307/1370059

Langfelder, P., Horvath, S. (2008). WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9,559. https://doi.org/10.1186/1471-2105-9-559

Peek, F. W. (1972). An experimental study of the territorial function of vocal and visual display in the male red-winged blackbird (Agelaius phoeniceus). Animal Behavior. 20, 112–118. https://doi.org/10.1016/S0003-3472(72)80180-5

Yasukawa, K., Lindsey-Robbins, J., Henger, C. S. & Hauber, M. E. (2016). Antiparasitic behaviors of red-winged blackbirds (Agelaius phoeniceus) in response to simulated brown-headed cowbirds (Molothrus ater): further tests of the frontloaded parasite-defense hypothesis. The Wilson Journal of Ornithology. 128, 475–486. https://doi.org/10.1676/1559-4491-128.3.475