An integrative mating system assessment of a nonmodel, economically important Pacific rockfish (Sebastes melanops) reveals nonterritorial polygamy and conservation implications for a large species flock

Abstract

Characterizing the mating systems of long‐lived, economically important Pacific rockfishes comprising the viviparous Sebastes species flock is crucial for their conservation. However, direct assignment of mating success to sires is precluded by open, offshore populations and high female fecundity. We addressed this challenge by integrating paternity‐assigned mating success of females with the adult sex ratio (ASR) of the population, male evolutionary responses to receptive females, and reproductive life history traits—in the framework of sexual selection theory—to assess the mating system of Sebastes melanops. Microsatellite parentage analysis of 17 pregnant females, 1,256 of their progeny, and 106 adults from the population yielded one to four sires per brood, a mean of two sires, and a female mate frequency distribution with a truncated normal (random) pattern. The 11 multiple paternity broods all contained higher median allele richness than the six single paternity broods (Wilcoxon test: W = 0, p < .001), despite similar levels of average heterozygosity. By sampling sperm and alleles from different males, polyandrous females gain opportunities to enhance their sperm supply and to lower the cost of mating with genetically incompatible males through reproductive compensation. A mean of two mates per mated female with a variance of one, an ASR = 1.2 females per male, and the expected population mean of 2.4 mates for mated males (and the estimated 35 unavailable sires), fits polygamous male mate frequency distributions that distinguish polygynandry and polyandrogyny mating systems, that is, variations of polygamy, but not polyandry. Inference for polygamy is consistent with weak premating sexual selection on males, expected in mid‐water, schooling S. melanops, owing to polyandrous mating, moderately aggregated receptive females, an even ASR, and no territories and nests used for reproduction. Each of these characteristics facilitates more mating males and erodes conspicuous sexual dimorphism. Evaluation of male evolutionary responses of demersal congeners that express reproductively territorial behavior revealed they have more potential mechanisms for producing premating sexual selection, greater variation in reproductive success, and a reduced breeding effective population size of adults and annual effective size of a cohort, compared to S. melanops modeled with two mates per adult. Such divergence in behavior and mating system by territorial species may differentially lower their per capita birth rates, subsequent population growth, and slow their recovery from exploitation.

Genetic evidence for the mating system and reproductive success of black sea bream (Acanthopagrus schlegelii)

“…Different mating systems vary in their sexual selection mechanisms (i.e., competition for mating through same‐sex combat and opposite‐sex mate choice), resulting in differences in the intensity and direction of sexual selection (i.e., greater on males or females) which affects the mating and reproductive success of a population (Arnold & Wade, 1984; Jones, 2009). Consequently, mating systems can drive morphological, behavioral, and physiological evolution, and create sexual conflict (Warner et al 1995; reviewed in Auld, 2018; Karageorge & Wilson, 2017). Many previous studies of mating systems have been based on observations of social behaviors, which can only explain the social mating system and not the genetic mating system, which specifies biological parentage of offspring (Jones & Ardren, 2003; Jones & Avise, 2001).…”

Multiple‐brooding rockfishes (Sebastes spp.) can utilize stored sperm from individual sires to fertilize consecutive broods

“…Multiple studies employing genetic paternity analysis have demonstrated that rockfishes can be polyandrous (documented in at least 15 species to date), with as many as four sires per brood observed in studies of wild fishes and as many as six sires per brood observed in studies of captive fishes (Gao et al ., 2017; Gray et al ., 2015; Hyde et al ., 2008; Johansson et al ., 2012; Karageorge & Wilson Jr., 2017; Sogard, Gilbert‐Horvath, et al ., 2008; Van Doornik et al ., 2008). This may be a diversified bet‐hedging strategy when mate selection criteria are uncertain (Yasui, 1998, Hyde et al ., 2008, Sogard, Gilbert‐Horvath, et al ., 2008, Johansson et al ., 2012).…”