Who are the missing parents? Grandparentage analysis identifies multiple sources of gene flow into a wild population

Abstract

In order to increase the size of declining salmonid populations, supplementation programmes intentionally release fish raised in hatcheries into the wild. Because hatchery-born fish often have lower fitness than wild-born fish, estimating rates of gene flow from hatcheries into wild populations is essential for predicting the fitness cost to wild populations. Steelhead trout (Oncorhynchus mykiss) have both freshwater resident and anadromous (ocean-going) life history forms, known as rainbow trout and steelhead, respectively. Juvenile hatchery steelhead that 'residualize' (become residents rather than go to sea as intended) provide a previously unmeasured route for gene flow from hatchery into wild populations. We apply a combination of parentage and grandparentage methods to a three-generation pedigree of steelhead from the Hood River, Oregon, to identify the missing parents of anadromous fish. For fish with only one anadromous parent, 83% were identified as having a resident father while 17% were identified as having a resident mother. Additionally, we documented that resident hatchery males produced more offspring with wild anadromous females than with hatchery anadromous females. One explanation is the high fitness cost associated with matings between two hatchery fish. After accounting for all of the possible matings involving steelhead, we find that only 1% of steelhead genes come from residualized hatchery fish, while 20% of steelhead genes come from wild residents. A further 23% of anadromous steelhead genes come from matings between two resident parents. If these matings mirror the proportion of matings between residualized hatchery fish and anadromous partners, then closer to 40% of all steelhead genes come from wild trout each generation. These results suggest that wild resident fish contribute substantially to endangered steelhead 'populations' and highlight the need for conservation and management efforts to fully account for interconnected Oncorhynchus mykiss life histories.

Anadromy and residency in steelhead and rainbow trout (Oncorhynchus mykiss): a review of the processes and patterns

“…Offspring from the above-waterfall resident population described earlier also produced significant numbers of smolts and returning anadromous adults despite over 70 years of complete selection against migration (see also Hayes et al 2012;. Likewise, freshwater maturation persists in many, if not all, hatchery steelhead trout stocks after decades of selectively breeding only anadromous adults (Christie et al 2011;Sharpe et al 2007;Sloat and Reeves 2014). Otolith microchemistry revealed that anadromous kelts in the Yakima River basin, Washington, had resident mothers 7% and 20% of the time in each of 2 years of study (Courter et al 2013).…”

“…Larger individuals attempt to dominate access to females through aggressive competition, whereas smaller individuals rely more on sneaking tactics to surreptitiously fertilize eggs during spawning (Fleming 1996). The size differences of males using alternative mating tactics can be great (Fleming and Reynolds 2004), though small sneaking males can still have significant reproductive success (Christie et al 2011;Martinez et al 2000;Morán et al 1996;Seamons et al 2004). Males therefore more frequently become residents because they are less dependent on large body size for reproductive success than females, and as a result, they mature across a much greater range of ages and sizes (Jonsson and Jonsson 1993;Roni and Quinn 1995).…”

“…For example, Christie et al (2011) demonstrated that resident fish contributed approximately 40% of the genes to Hood River, Oregon, steelhead populations. In the study by , progeny from all possible combinations of anadromous and resident crosses exhibited similar mean rates of freshwater maturation.…”

“…For example, greater life history diversity in O. mykiss spreads mortality risk over space and time, thereby dampening population fluctuations and increasing resiliency to environmental variability (Moore et al 2014). Further, resident males mating with anadromous females (McMillan et al 2007) and the contribution of anadromous offspring from residents and vice-versa (Christie et al 2011;Courter et al 2013;Sloat and Reeves 2014) offer important avenues for buffering genetic and demographic stochasticity that are much less available to other Pacific salmonines . Declines in the anadromous component of O. mykiss populations in the United States, Canada, and Russia have motivated an increased interest in exploring the factors shaping anadromy and residency, especially as changing climate conditions and anthropogenic activities alter the fitness of these different forms (Benjamin et al 2013;Satterthwaite et al 2010).…”

“…"Steelhead" and "rainbow trout" are the common North American names for anadromous and freshwater resident life history forms of O. mykiss, respectively, whereas both forms are known as "mykizha" in Russia. Anadromous and resident forms are often sympatric, commonly interbreed, and their offspring may adopt either form (Christie et al 2011;Courter et al 2013;Sloat and Reeves 2014). The balance of life histories can vary, with some populations supporting more residents and others more anadromous individuals (e.g., .…”