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

• Published in: Ecology and evolution Vol. 7; no. 24; pp. 11277 - 11291
• Main Authors: Karageorge, Kurt W., Wilson, Raymond R.
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01-12-2017; John Wiley and Sons Inc
• Subjects: Adults; Alkali-silica reactions; Alleles; Animal behavior; Animal reproduction; Breeding; Breeding success; Congeners; Conservation; Divergence; Economic conditions; Exploitation; Fecundity; Females; Fish; Frequency distribution; genetic incompatibility; Heterozygosity; Life history; Males; Mating behavior; Microsatellites; Nests; Original Research; Paternity; polyandrogyny; polyandrous females; Polyandry; Polygamy; polygynandry; Population; Population growth; Population number; premating; Progeny; Reproduction; Sebastes melanops; Sex ratio; Sexual behavior; Sexual dimorphism; Sexual selection; Sperm; Success; Territorial behavior; Viviparity‐Driven Conflict Hypothesis; Wildlife conservation; sexual selection; Viviparity‐Driven Conflict Hypothesis; polyandrogyny; polyandrous females; premating; genetic incompatibility; polygynandry
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.3579

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.
Our mating system assessment of a nonmodel, exploited marine fish (Sebastes melanops) estimated mate frequency parameters from pregnant females, their offspring, and adults in the breeding population to conclude that polygamy is common in both sexes. This finding is consistent with our evaluations of male evolutionary responses to female receptivity for S. melanops and congeners with a mid‐water, schooling, and nonterritorial life history as adults, and with weak expected premating directional sexual selection on males; all support a nonterritorial polygamy mating system classification for S. melanops. Our evaluation of benthic congeners that express reproductively territorial behavior revealed they have more potential mechanisms for producing premating sexual selection and a reduced annual Ne to cohorts (due to a reduction in their birth rates). An associated reduction in population growth may slow their recovery from exploitation, compared to same‐sized adult populations of S. melanops modeled with two mates per adult.