The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex–color combinations
Wood, Chelsea et al. (2021), The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex–color combinations, Dryad, Dataset, https://doi.org/10.5061/dryad.83bk3j9sr
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.
Lingcod (n = 2,251) were collected between 2015 and 2017 using hook-and-line methods from chartered commercial passenger fishing vessels (CPFVs) from Yakutat, Alaska to San Diego, California, USA (54°30'N–34°30’N). The following seven regions were broadly identified: Southeast Alaska (54°30'N–59°48'N), Puget Sound and coastal Washington (46°16’N–49°N), Oregon (42°N–46°16’N), northern California (38°02’N–42°N), central California (34°30’N–38°02’N), and southern California (32°32’N–34°30’N; Figure 2). Note that samples for parasitological analysis were drawn from only four of these seven regions, spanning most of the geographic range: Southeast Alaska, Washington, northern California, and southern California. Three to four fishing ports were selected per region (n = 24 ports total) based on location and accessibility of CPFVs. To ensure representation of lingcod across a wide range of size and age classes, we sampled shallow (<200 ft) and deep (200–550 ft) nearshore and offshore rocky reefs equally. On average, we fished for 2.5 days out of each port at different locations (shallow and deep) to obtain the targeted sample size of 75–100 lingcod per port. Additional samples were provided by the Alaska commercial longline fishery, the NWFSC Rockfish Bycatch Study in Puget Sound, the Oregon Department of Fish and Wildlife Marine Reserves Program, and the California Collaborative Fisheries Research Program. With the exception of lingcod collected by the Alaska commercial longline fishery, sampling design from all other lingcod collection methods are similar to that of the current study, with respect to chartering CPFVs for single day trips, using volunteer anglers, and targeting nearshore fishing grounds.
We measured several phenotypic traits for each of the lingcod included in the coastwide dataset. Color was recorded as blue or brown immediately upon capture, then reassessed in the lab (as chromatophores on fish skin are known to undergo apoptosis, causing external color to change upon death). Color was determined internally based on muscle tissue and fin membrane coloration, as well as externally based on skin color. There was an observed gradient in “blueness” (Figure 1a), but color was noted as binary (brown or blue). If there was disagreement between internal and external coloration, we used the internal color, as it may represent a stronger phenotypic expression of the blue trait. To our knowledge, there is no scholarship on the process of post-mortem color degradation in lingcod, but we do know that internal blue coloration persists after death, because blue filets are sold in seafood markets and fetch a higher price than the more typical white filets; in fact, among seafood processors, it is known that blue coloration will remain in blue filets until cooking. For this reason, we use internal coloration to demarcate blue from brown individuals. Sex was determined externally (based on the presence or absence of a conical papilla) and internally (based on the presence of ovaries or testes). Total length was measured to the nearest 0.1 cm and total mass was measured to the nearest 0.01 kg. Internal organs were removed so that gonad mass could be measured to the nearest 0.0001 kg and liver mass to the nearest 0.0001 kg.
Parasitological dissection of lingcod
Within the coastwide group of lingcod, we sub-sampled 89 for parasitological study. These individuals were immediately measured and bagged upon capture to retain external parasites, which can otherwise drop off their host after death. For each of the 89 fish selected for parasitological dissection, we performed a comprehensive parasitological examination designed to detect most metazoan parasites. Processing time per fish ranged from 4 to 30 hours and averaged 16 hours. We did not search for myxozoan parasites, but all other metazoan parasites should have been detected by our standard parasitological dissection techniques (described in detail in the manuscript). We identified all parasite taxa to the lowest possible taxonomic level using keys, host–parasite checklists, regional parasite identification guides, and primary literature.
NOAA NMFS Habitat Assessment Improvement Plan, Award: NA15-NMF4550353
National Science Foundation, Award: OCE-1829509
Alfred P. Sloan Foundation
UW President's Innovation Imperative
UW Royalty Research Fund