skip to main content


Title: The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex–color combinations
The unusual blue color polymorphism of lingcod ( Ophiodon elongatus ) is the subject of much speculation but little empirical research; ~20% of lingcod individuals exhibit this striking blue color morph, which is discrete from and found within the same populations as the more common brown morph. In other species, color polymorphisms are intimately linked with host–parasite interactions, which led us to ask whether blue coloration in lingcod might be associated with parasitism, either as cause or effect. To test how color and parasitism are related in this host species, we performed parasitological dissection of 89 lingcod individuals collected across more than 26 degrees of latitude from Alaska, Washington, and California, USA. We found that male lingcod carried 1.89 times more parasites if they were blue than if they were brown, whereas there was no difference in parasite burden between blue and brown female lingcod. Blue individuals of both sexes had lower hepatosomatic index (i.e., relative liver weight) values than did brown individuals, indicating that blueness is associated with poor body condition. The immune systems of male vertebrates are typically less effective than those of females, due to the immunocompromising properties of male sex hormones; this might explain why blueness is associated with elevated parasite burdens in males but not in females. What remains to be determined is whether parasites induce physiological damage that produces blueness or if both blue coloration and parasite burden are driven by some unmeasured variable, such as starvation. Although our study cannot discriminate between these possibilities, our data suggest that the immune system could be involved in the blue color polymorphism–an exciting jumping-off point for future research to definitively identify the cause of lingcod blueness and a hint that immunocompetence and parasitism may play a role in lingcod population dynamics.  more » « less
Award ID(s):
1829509
NSF-PAR ID:
10353804
Author(s) / Creator(s):
; ; ; ; ; ;
Editor(s):
Lutermann, Heike
Date Published:
Journal Name:
PLOS ONE
Volume:
16
Issue:
12
ISSN:
1932-6203
Page Range / eLocation ID:
e0261202
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Climate‐modulated parasitism is driven by a range of factors, yet the spatial and temporal variability of this relationship has received scant attention in wild vertebrate hosts. Moreover, most prior studies overlooked the intraspecific differences across host morphotypes, which impedes a full understanding of the climate–parasitism relationship. In the common lizard (Zootoca vivipara), females exhibit three colour morphs: yellow (Y‐females), orange (O‐females) and mixed (mixture of yellow and orange, M‐females).Zootoca viviparais also infested with an ectoparasite (Ophionyssusmites). We therefore used this model system to examine the intraspecific response of hosts to parasitism under climate change. We found infestation probability to differ across colour morphs at both spatial (10 sites) and temporal (20 years) scales: M‐females had lower parasite infestations than Y‐ and O‐females at lower temperatures, but became more susceptible to parasites as temperature increased. The advantage of M‐females at low temperatures was counterbalanced by their higher mortality rates thereafter, which suggests a morph‐dependent trade‐off between resistance to parasites and host survival. Furthermore, significant interactions between colour morphs and temperature indicate that the relationship between parasite infestations and climate warming was contingent on host morphotypes. Parasite infestations increased with temperature for most morphs, but displayed morph‐specific rates. Finally, infested M‐females had higher reductions in survival rates than infested Y‐ or O‐females, which implies a potential loss of intraspecific diversity within populations as parasitism and temperatures rise. Overall, we found parasitism increases with warming temperatures, but this relationship is modulated by host morphotypes and an interaction with temperature. We suggest that epidemiological models incorporate intraspecific diversity within species for better understanding the dynamics of wildlife diseases under climate warming.

     
    more » « less
  2. Abstract

    Variation in color morph behavior is an important factor in the maintenance of color polymorphism. Alternative anti-predator behaviors are often associated with morphological traits such as coloration, possibly because predator-mediated viability selection favors certain combinations of anti-predator behavior and color. The Aegean wall lizard,Podarcis erhardii, is color polymorphic and populations can have up to three monochromatic morphs: orange, yellow, and white. We investigated whether escape behaviors differ among coexisting color morphs, and if morph behaviors are repeatable across different populations with the same predator species. Specifically, we assessed color morph flight initiation distance (FID), distance to the nearest refuge (DNR), and distance to chosen refuge (DR) in two populations of Aegean wall lizards from Naxos island. We also analyzed the type of refugia color morphs selected and their re-emergence behavior following a standardized approach. We found that orange morphs have different escape behaviors from white and yellow morphs, and these differences are consistent in both populations we sampled. Orange morphs have shorter FIDs, DNRs, and DRs; select different refuge types; and re-emerge less often after being approached compared to white and yellow morphs. Observed differences in color morph escape behaviors support the idea that morphs have evolved alternative behavioral strategies that may play a role in population-level morph maintenance and loss.

    Significance statement

    Color polymorphic species often differ in behaviors related to reproduction, but differences in other behaviors are relatively underexplored. In this study, we use an experimental approach in two natural populations of color populations of color polymorphic lizards to determine that color morphs have diverged in their escape behaviors. By conducting our experiments in two different populations with similar predator regimes, we show for the first time that behavioral differences among intra-specific color morphs are repeatable across populations, suggesting that alternative behavioral strategies have evolved in this species. Using this experimental approach, we demonstrate that the brightest orange morph stays closer to refuge than other morphs, uses a different refuge type (vegetation) more often than other morphs (wall crevices), and take much longer to emerge from refuge after a simulated predation event than other morphs. Thus, selective pressures from visual predators may differ between morphs and play a role in the evolution and maintenance of color polymorphisms in these types of systems. Our study species,Podarcis erhardii, belongs to a highly color polymorphic genus (19/23 spp. are color polymorphic) that contains the same three color morphs, thus we believe our results may be relevant to more than justP.erhardii.

     
    more » « less
  3. null (Ed.)
    Research on the ‘ecology of fear’ posits that defensive prey responses to avoid predation can cause non-lethal effects across ecological scales. Parasites also elicit defensive responses in hosts with associated non-lethal effects, which raises the longstanding, yet unresolved question of how non-lethal effects of parasites compare with those of predators. We developed a framework for systematically answering this question for all types of predator–prey and host–parasite systems. Our framework reveals likely differences in non-lethal effects not only between predators and parasites, but also between different types of predators and parasites. Trait responses should be strongest towards predators, parasitoids and parasitic castrators, but more numerous and perhaps more frequent for parasites than for predators. In a case study of larval amphibians, whose trait responses to both predators and parasites have been relatively well studied, existing data indicate that individuals generally respond more strongly and proactively to short-term predation risks than to parasitism. Apart from studies using amphibians, there have been few direct comparisons of responses to predation and parasitism, and none have incorporated responses to micropredators, parasitoids or parasitic castrators, or examined their long-term consequences. Addressing these and other data gaps highlighted by our framework can advance the field towards understanding how non-lethal effects impact prey/host population dynamics and shape food webs that contain multiple predator and parasite species. 
    more » « less
  4. Many avian species are negatively impacted by obligate avian brood parasites, which lay their eggs in the nests of host species. The yellow warbler (Setophaga petechia), which is host to the brood-parasitic brown-headed cowbird (Molothrus ater), represents one of the best-replicated study systems assessing antiparasitic host defenses. Over 15 prior studies on yellow warblers have used model-presentation experiments, whereby breeding hosts are exposed to models of brown-headed cowbirds or other nest threats, to test for anti-parasitic defenses unique to this species. Here we present results from our own quasi-replication study of the yellow warbler/brown-headed cowbird system, which used a novel design compared to previous experiments by pivoting to conduct acoustic playback treatments only, rather than presenting visual models with or without calls. We exposed active yellow warbler nests to playbacks of brown-headed cowbird chatters (brood parasite), blue jay (Cyanocitta cristata; nest predator) calls, conspecific “seet” calls (a referential alarm call for brood parasitism risk), conspecific “chip” calls (a generic alarm call), or control wood thrush (Hylocichla mustelina; harmless heterospecific) songs during the incubation stage. Similar to previous studies, we found that female yellow warblers seet called more frequently in response to playbacks of both brood parasitic chatter calls and conspecific seet calls whereas they produced more chip calls in response to the playback of nest predator calls. In contrast, female yellow warblers approached all playbacks to similar distances, which was different from the proximity patterns seen in previous studies. Our study demonstrates the importance of both replicating, and also pivoting, experimental studies on nest defense behaviors, as differences in experimental design can elicit novel behavioral response patterns in the same species. 
    more » « less
  5. Long-term data allow ecologists to assess trajectories of population abundance. Without this context, it is impossible to know whether a taxon is thriving or declining to extinction. For parasites of wildlife, there are few long-term data—a gap that creates an impediment to managing parasite biodiversity and infectious threats in a changing world. We produced a century-scale time series of metazoan parasite abundance and used it to test whether parasitism is changing in Puget Sound, United States, and, if so, why. We performed parasitological dissection of fluid-preserved specimens held in natural history collections for eight fish species collected between 1880 and 2019. We found that parasite taxa using three or more obligately required host species—a group that comprised 52% of the parasite taxa we detected—declined in abundance at a rate of 10.9% per decade, whereas no change in abundance was detected for parasites using one or two obligately required host species. We tested several potential mechanisms for the decline in 3+-host parasites and found that parasite abundance was negatively correlated with sea surface temperature, diminishing at a rate of 38% for every 1 °C increase. Although the temperature effect was strong, it did not explain all variability in parasite burden, suggesting that other factors may also have contributed to the long-term declines we observed. These data document one century of climate-associated parasite decline in Puget Sound—a massive loss of biodiversity, undetected until now. 
    more » « less