Linking mating preferences to sexually selected traits and offspring viability: good versus complementary genes hypotheses

Abstract

Indirect-fitness benefits hypotheses suggest that offspring of preferred mates should exhibit greater survival or reproductive success. For example, good-genes hypotheses propose that female mating preferences are mediated by secondary sexual traits because they honestly reflect the ability to pass on genes that will enhance offspring survival or reproduction. Conversely, complementary-genes hypotheses propose that mating preferences are mediated by complementary-genes because they enhance offspring viability. While these two research traditions are not strict alternatives and both may operate simultaneously, they have never been tested together. Here we explore the multiple potential underlying factors influencing mating preference evolution in Jamaican field crickets, Gryllus assimilis. After evaluating female preferences for randomly selected males, we tested if preferred males differed from nonpreferred males in their body size, relative mass, or mate attraction signals. We then mated females to their preferred or non-preferred partners and tested offspring viability. Results revealed: (1) females preferred larger males, (2) larger females oviposited more eggs, (3) neither morphology nor mate attraction signaling explained variation in offspring viability, and (4) mating with a preferred partner did not enhance offspring viability. Overall, in our current study population, cricket mate preferences were inconsistent with complementary-genes and goodgenes hypotheses for indirect-fitness-benefits. Our current research explores whether male secondary sexual traits honestly reflect the ability to pass on genes that enhance offspring reproduction. or the attractiveness of sons in the subsequent generation (Fisher 1930; Zahavi 1975; Heywood 1989; Andersson 1994). For example, Fisher (1930) and later Zahavi (1975) posited that secondary sexual traits reflect their bearers' health and viability (good-genes). When both secondary sexual traits and female preferences are heritable, females that mate with more elaborate males (males with brighter, louder, or more complex secondary sexual traits) will produce offspring that may inherit their father's good-genes for health and viability, and their mothers' good-genes for preference, resulting in greater survival and/or reproductive success. A correlation may result between preference and viability [demonstrated by Lande (1981)]. The difficulty with these hypotheses is that continuous directional selection for elaborate traits may remove heritable variation, resulting in the elimination of the indirect benefits associated with mate preference (e.g. Falconer and Mackay 1996; Borgia 1979; Andersson 1994; but see Heywood 1989; Pomiankowski 1988). The main rationale for Hamilton and Zuk's (1982) insightful paper on mate choice was to with laboratory rearing, cricket care, egg counting and morphological measurements. We thank

What is driving male mate preference evolution in Jamaican field crickets?

“…There was a non‐significant trend for smaller G. assimilis females to oviposit more eggs than larger females. This negative trend was unexpected, given previous studies revealed larger G. assimilis females are more fecund (e.g., Bertram & Rook, ; Bertram et al., ; Loranger & Bertram, ), a relationship found in almost all field crickets studied to date (e.g., G. bimaculatus : Bateman et al., ; G. texensis : Shoemaker, ; Teleogryllus oceanicus : Simmons & Garcia‐Gonzalez, ; G. integer : Hedrick & Kortet, ; G. assimilis : Bertram et al., ; Loranger & Bertram, ). Our suspicion is that larger G. assimilis females did, in fact, have higher “potential” for offspring production, but they did not allocate all their eggs according to their potential, as they were not allowed to perform free mate choice or mate multiply as they would have in the wild.…”

“…Mating treatment did not influence the number of eggs oviposited. Female field crickets exhibit extensive unexplained variation in their fecundity (Bertram et al., ; Bradford, Guerette, & Roff, ; Bretman et al., ; Carriére & Roff, ; Shoemaker, ; Simmons & Garcia‐Gonzalez, ; Simmons et al., ; Stahlschmidt & Adamo, ; Stahlschmidt, O'Leary, & Adamo, ; Tregenza & Wedell, ; Tuni et al., ). For example, in our study, females ranged from ovipositing 0–682 eggs; ± SE = 325 ± 28, CV = 67.…”

“…We conducted our study in accordance with the guidelines of the Canadian Council on Animal Care. Detailed methods are provided in our two companion papers (Bertram et al., ; Susan M. Bertram, Michelle J. Loranger, Ian R. Thomson, Sarah J. Harrison, Genevieve L. Ferguson, Mykell L. Reifer, Deborah H. Corlett, & Patricia Adair Gowaty, submitted). We used laboratory‐reared G. assimilis field crickets descended from wild crickets captured in Smithville, Texas, from September 15 to 24, 2007.…”

“…For example, female crickets bias their sperm storage and paternity toward unrelated versus related males when the opportunity arises (Bretman, Wedell, & Tregenza, ; Simmons, Beveridge, Wedell, & Tregenza, ; Tregenza & Wedell, ; Tuni, Beveridge, & Simmons, ). Conversely, there is also evidence that male mate choice may not mediate offspring viability, as our recent research on female mate choice revealed that offspring viability was not significantly higher when females were mated to their preferred‐ versus their non‐preferred mate (Bertram et al., ). To test this indirect‐benefits hypothesis, we therefore quantified whether offspring viability (egg hatching success and juvenile to adult molting success) was higher when males were mated to their preferred versus non‐preferred female partner.…”

“…Benefits from increased egg number could mediate male mating preference evolution, as male crickets often preferentially court larger females when given the opportunity (Bateman & Fleming, ), and larger females often oviposit more eggs than smaller females (Bateman, Gilson, & Ferguson, ; Bertram et al., ; Bonduriansky, ; Hedrick & Kortet, ; Loranger & Bertram, ; Shoemaker, ; Simmons & Garcia‐Gonzalez, ). However, male mating preferences may be mediated by factors other than female body size (Susan M. Bertram, Michelle J. Loranger, Ian R. Thomson, Sarah J. Harrison, Genevieve L. Ferguson, Mykell L. Reifer, Deborah H. Corlett, & Patricia Adair Gowaty, submitted).…”