An obligate brood parasite trapped in the intraspecific arms race of its hosts

Abstract

Reciprocal selection pressures often lead to close and adaptive matching of traits in coevolved species. A failure of one species to match the evolutionary trajectories of another is often attributed to evolutionary lags or to differing selection pressures across a geographic mosaic. Here we show that mismatches in adaptation of interacting species--an obligate brood parasitic duck and each of its two main hosts--are best explained by the evolutionary dynamics within the host species. Rejection of the brood parasite's eggs was common by both hosts, despite a lack of detectable cost of parasitism to the hosts. Egg rejection markedly reduced parasite fitness, but egg mimicry experiments revealed no phenotypic natural selection for more mimetic parasitic eggs. These paradoxical results were resolved by the discovery of intraspecific brood parasitism and conspecific egg rejection within the hosts themselves. The apparent arms race between species seems instead to be an incidental by-product of within-species conflict, with little recourse for evolutionary response by the parasite.

Interspecific egg rejection as ecological collateral damage from selection driven by conspecific brood parasitism

“…Given this reduced parasitic virulence, one might expect somewhat benign interactions between the brood parasite and its hosts. However, our previous study in Argentina revealed that duck eggs are often rejected by the two main hosts, the red-gartered coot, Fulica armillata, and the redfronted coot, Fulica rufifrons (Figure 1), despite a lack of detectable costs of parasitism imposed by the ducks (Lyon & Eadie, 2004). Moreover, parasite and host eggs differ strikingly in appearance (Figure 2), yet an experimental study revealed that increasingly mimetic eggs do not alter rejection rates (Lyon & Eadie, 2004).…”

“…However, our previous study in Argentina revealed that duck eggs are often rejected by the two main hosts, the red-gartered coot, Fulica armillata, and the redfronted coot, Fulica rufifrons (Figure 1), despite a lack of detectable costs of parasitism imposed by the ducks (Lyon & Eadie, 2004). Moreover, parasite and host eggs differ strikingly in appearance (Figure 2), yet an experimental study revealed that increasingly mimetic eggs do not alter rejection rates (Lyon & Eadie, 2004). These paradoxical findings, coupled with the subsequent discovery of conspecific brood parasitism and rejection of conspecific parasitic eggs in both species of hosts, led us to conclude that the rejection of duck eggs is likely to be an incidental by-product of natural selection on hosts to recognize and reject the eggs of conspecifics (Lyon & Eadie, 2004).…”

“…Although the tendency is to often assume that interspecific parasitism is the evolutionary driver of host traits, perhaps because interspecific parasitism is often more obvious and easily detected than conspecific parasitism, it is possible that some signatures of coevolution might instead be fuelled by the brood parasitism within the hosts themselves (Freeman, 1988;Lahti, 2006;Lyon and Eadie, 2004). In these taxa it has proven difficult to disentangle the relative roles of conspecific and interspecific brood parasitism as drivers of host defenses (Freeman, 1988;Grendstad et al, 1999;Jackson, 1992;Lahti, 2006;Peer et al, 2007;Rothstein, 2001;Samas et al, 2014).…”

“…Moreover, parasite and host eggs differ strikingly in appearance (Figure 2), yet an experimental study revealed that increasingly mimetic eggs do not alter rejection rates (Lyon & Eadie, 2004). These paradoxical findings, coupled with the subsequent discovery of conspecific brood parasitism and rejection of conspecific parasitic eggs in both species of hosts, led us to conclude that the rejection of duck eggs is likely to be an incidental by-product of natural selection on hosts to recognize and reject the eggs of conspecifics (Lyon & Eadie, 2004). Unlike the ducklings, which feed themselves, coot chicks are fed by their parents.…”

“…Black-headed ducks are unique among the 101 species of avian obligate brood parasites in that their young are precocial and, unlike all other brood parasites, they leave the nest upon hatching and make no posthatching demands on the parental care of their hosts (Davies, 2000;Lyon and Eadie, 2004;Lyon and Eadie, 2013;Weller, 1968). Given this reduced parasitic virulence, one might expect somewhat benign interactions between the brood parasite and its hosts.…”