Abstract
Sexual reproduction brings together reproductive partners whose long‐term interests often differ, raising the possibility of conflict over their reproductive investment. Males that enhance maternal investment in their offspring gain fitness benefits, even if this compromises future reproductive investment by iteroparous females. When the conflict occurs at a genomic level, it may be uncovered by crossing divergent populations, as a mismatch in the coevolved patterns of paternal manipulation and maternal resistance may generate asymmetric embryonic growth. We report such an asymmetry in reciprocal crosses between populations of the fish Girardinichthys multiradiatus. We also show that a fragment of a gene which can influence embryonic growth (Insulin‐Like Growth Factor 2; igf2) exhibits a parent‐of‐origin methylation pattern, where the maternally inherited igf2 allele has much more 5′ cytosine methylation than the paternally inherited allele. Our findings suggest that male manipulation of maternal investment may have evolved in fish, while the parent‐of‐origin methylation pattern appears to be a potential candidate mechanism modulating this antagonistic coevolution process. However, disruption of other coadaptive processes cannot be ruled out, as these can lead to similar effects as conflict.
Highlights
We demonstrate an interaction between paternal and maternal origin in the size attained at birth by G. multiradiatus offspring
Differences between parental and hybrid phenotypes can be the consequence of maternal effects if, for instance, females perceive the males from the alternative populations to be more attractive than those from their own, and preferentially invest in offspring of attractive males (Burley, 1988; Gil et al, 1999)
This is unlikely to explain our results as females from both localities are reluctant to mate with males from the other population (González Zuarth & Macías Garcia, 2006) unless they are raised together from an early age (De Gasperin & Macías Garcia, 2014)
Summary
The Amarillo (Figure 1) is found in water bodies of the upper Lerma River basin, and in limited upland regions of the adjacent Balsas and Pánuco catchments (Gesundheit & Macias-Garcia, 2005). To determine whether the asymmetric effects on offspring size could be influenced by parent-of-origin effects in the methylation state of igf, we took advantage of a heterozygous C/T embryo (P21- 3) that inherited a T allele from its mother and a C allele from its father, and of a heterozygous C/T adult female (P11-F)— here we did not know the parental origin of each allele—and analyzed the pattern of 5′ cytosine methylation in a 443-bp fragment that spanned the SNP site by treating genomic DNA with bisulfite before PCR amplification and cloning. We observed a similar pattern with offspring width, with no effect of female population (F(1,65.2) = 0.94, p = .34), and a significant male X female interaction (F(1,65.2) = 4.51, p = .04); offspring of Z-M were wider than those from Z-Z crosses (Bonferroni F(1,63.5) = 7.14, p = .02; Figure 3b).
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