DISCUSSION
Using a parentage-based tagging approach we have provided the first
description of the genetic mating system for Yellowstone Cutthroat
Trout, a species of conservation concern and recreational angling
importance. We documented multiple forms of mating among adults
including monogamy, polygyny, and polyandry, and offspring production
was found to be heavily right skewed with few adults producing many and
most producing few or no offspring. The variance in relative
reproductive success was higher among males than females as measured
both by the number of mates acquired and number of offspring produced.
We observed a positive correlation between the number of mates acquired
and relative number of offspring produced; however, the strength of this
correlation was lower for females than for males. On average, male
adults had a greater number of mates and produced a higher number of
offspring than their female counterparts. We failed to detect a signal
of inbreeding avoidance, although the group of parents that produced
progeny were on average slightly less related than adults that did not
produce progeny. Both arrival date and total length were identified as
significant predictors of relative reproductive success for both female
and male Yellowstone Cutthroat Trout. Lastly, we identified that the
effective number of breeders was lower than effective populations and
these two parameter estimates had non-overlapping confidence intervals.
Combined, the current study of Yellowstone Cutthroat Trout mating system
helps to fill several gaps in knowledge regarding life history and these
data may be useful moving forward for conservation and management
efforts.
Social mating systems and spawning behaviors are well studied within
salmonids (see Esteve 2005 for review); however, there remain taxa for
which there is little or no information, including Cutthroat Trout.
Several traits observed in our study of Yellowstone Cutthroat Trout were
in line with patterns described for other members of the Salmonidae
family. For example, we found evidence of both polygamous and monogamous
matings, an observation that has been noted for Steelhead (Seamons et
al. 2004a), Brown Trout (Salmo trutta , Serbezov et al. 2010), and
Brook Trout (Kanno et al. 2011). In Chinook Salmon (O.
tshawytscha ) and Atlantic Salmon, there is evidence of polyandry but
not polygyny (Bentzen et al. 2001; Fleming 1998). Theoretical
expectations are that polygamy would be a common occurrence among
salmonids because one sex is free of parental care (males) and
intrasexual selection in the form of male-male competition is strong (de
Gaudemar et al. 1998). Thus, it was not necessarily unexpected for us to
observe polygamy and monogamy in Yellowstone Cutthroat Trout. From a
management perspective, these findings are important as multiple
paternity (or polyandry) has been shown to increase effective population
size (N e) relative to systems with strict
monogamy (Pearse and Anderson 2010). It is worth noting that the parent
pair-offspring relationships identified via PBT which were used to infer
mating systems displayed a high level of concordance with results from
sibship analysis. Our findings mirror previous efforts to resolve
full-sibling families via sibship methods (Ackerman et al. 2016), and
highlight that it is possible to accurately estimate sibship andN b without parental genotypes (Waples and Waples
2011). The ability to infer family structure using only offspring from a
single generation is significant as it can be applied in scenarios where
sampling both parents and their offspring is either logistically
difficult or not possible.
Another trait observed in Yellowstone Cutthroat Trout that mirrors
observations from other salmonids was protandry, whereby males arrived
earlier than females to spawning grounds. Although male Yellowstone
Cutthroat Trout arrived earlier to spawning grounds than females
(Figure 4A ), the cumulative number of offspring assigned to
males was highest among those that arrived midseason (Figure
4B ). Protandry has been widely documented in Pacific salmon (Morbey
2000) and Steelhead (McMillan et al. 2007, although see Seamons et al.
2004b) and it has been hypothesized that males arrive early to establish
dominant access to spawning females (e.g., Healey and Prince 1998). The
ability for males to establish dominance over competing males can be
influenced by body size (Quinn & Foote1994; Fleming 1998; Dickerson et
al. 2002), prior residence (Foote 1990), and the ratio of sexually
active females to males (e.g., operational sex ratio; OSR). Results from
our generalized linear models identified both arrival date and total
length as significant predictors of relative reproductive success on an
individual basis. In other words, while the bulk of offspring were
collectively assigned to males that arrived mid-season (Figure
4B ), early arriving males that were larger in size had the highest
individual relative offspring production (Figure 5 ). There are
numerous examples in the salmon literature of reproductive success being
positively related to body size (e.g., Schroeder 1981; Fleming and Gross
1992; Quinn and Foote 1994; Fleming 1996; Seamons et al. 2004b;
Berejikian et al. 2009; Anderson et al. 2012); however, there are other
instances where the relationship is either weak, non-existent, or
affected by other forms of selection (e.g., Seamons et al. 2004b;
Dickerson et al. 2005; Seamons et al. 2007). Whereas different life
history strategies (e.g., precocial males and jacks), behavioral
strategies (e.g., sneaker or satellite males), and forms of selection
(e.g., predation by terrestrial animals) may lessen the strength of the
relationship between arrival time and body size on reproductive success
(Dickerson et al. 2002; Dickerson et al. 2005; MacMillan et al. 2007),
in our system the largest, earliest arriving males experienced the
highest levels of relative reproductive success.
Pairwise genetic relatedness among adult Yellowstone Cutthroat Trout
that successfully mated was not significantly different relative to
adults that did not successfully reproduce, and this trend has been
noted for other salmonids. Several studies have identified mate choice
among salmonids, specifically at loci associated with the major
histocompatibility class (MHC). In particular, both Atlantic Salmon and
Chinook Salmon have been shown to select mates that increase
heterozygosity at the MHC loci, but not at putatively neutral loci
(Landry et al. 2001; Neff et al. 2008). Because we only surveyed
Yellowstone Cutthroat Trout at putatively neutral SNP loci we were
unable to test for mate association at MHC, but nonetheless, we showed
patterns of genetic relatedness among parents supported a random mating
scheme.
Lastly, we generated estimates of N b andN e and showed that theN b/N e was less than one
for Yellowstone Cutthroat Trout. Ratios ofN b/N e vary across
freshwater fish (Brown Trout: 0.48, Lake Trout, Salvelinus
namaycush : 1.212, Razorback Sucker, Xyrauchen texanus : 1.004)
and simple life history characteristics such as age at maturity and
adult lifespan have been shown to explain up to 2/3 of the variation in
observed N b/N e ratios
(Waples et al. 2013). In the case of Yellowstone Cutthroat Trout in the
South Fork Snake River, there are two pools of potential parents capable
of contributing to annual reproduction: tributary residents and mainstem
adults that perform fluvial spawning migrations (Thurow et al. 1988).
That we observed N b/N eratios less than one could be explained by only a subset of the
potential parent population contributing to reproduction (i.e., reduced
resident or fluvial contributions), an unusually large variance in
reproductive success, or a highly skewed operational sex ratio that
occurred in 2016 relative to other spawn years. Because we only have
data for a singular spawn year it is difficult to identify specific
mechanisms to explain our observedN b/N e ratio, but
nonetheless, both these values are sufficiently high to suggest that
Yellowstone Cutthroat Trout in Burns Creek represent a genetically
stable and diverse population.
In conclusion, we have described the mating systems of a species of
conservation concern and identified important predictors of relative
reproductive success. Moving forward, these data can serve as a baseline
for future monitoring efforts and a template for investigations into the
reproductive ecology of other freshwater salmonids. Additionally, the
observation that the largest adults were responsible for producing a
disproportionate amount of offspring may serve as a basis for angling
restrictions. For example, Gwinn et al. (2015) identified that
protection of the largest adults in the population via harvest slots
(i.e., harvest is restricted to fish of intermediate length)
consistently produced greater numbers of fish harvested and greater
catches of trophy fish while conserving reproductive biomass and a more
natural population age-structure. Throughout much of their range in
Idaho (including the South Fork Snake River and its tributaries), the
harvest of Yellowstone Cutthroat Trout is prohibited, but in areas where
harvest is still allowed or is being considered, data generated here may
be of direct relevance.