DOI: 10.5061/dryad.83bk3j9sr
title: The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex–color combinations

description: 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.
description: Lingcod
 collection 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; <b>Figure 2</b>). 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 (&lt;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”
 (<b>Figure 1a</b>), 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.