Developmental rate displays effects of inheritance but not of sex in interpopulation hybrids of Tigriopus californicus

Coevolved genetic interactions within populations can be disrupted by hybridization resulting in loss of fitness in hybrid individuals (i.e., hybrid breakdown). However, the extent to which variation in fitness-related traits among hybrids is inherited across generations remains unclear, and variation in these traits may be sex-specific in hybrids due to differential effects of genetic incompatibilities in females and males. Here we present two experiments investigating variation in developmental rate among reciprocal inter-population hybrids of the intertidal copepod Tigriopus californicus. Developmental rate is a fitness-related trait in this species that is affected by interactions between mitochondrial-encoded and nuclear-encoded genes in hybrids that result in variation in mitochondrial ATP synthesis capacities. First, we show that F2-hybrid developmental rate is equivalent in two reciprocal crosses and is unaffected by sex, suggesting that breakdown of developmental rate is likely experienced equally by females and males. Second, we demonstrate that variation in developmental rate among F3 hybrids is heritable; times to copepodid metamorphosis of F4 offspring of fast-developing F3 parents (12.25 ± 0.05 d, μ ± SEM) were significantly faster than those of F4 offspring of slow-developing parents (14.58 ± 0.05 d). Third, we find that ATP synthesis rates in these F4 hybrids are unaffected by the developmental rates of their parents, but that mitochondria from females synthesize ATP at faster rates than mitochondria from males. Taken together, these results suggest that sex-specific effects vary among fitness-related traits in these hybrids and that effects likely associated with hybrid breakdown display substantial inheritance across hybrid generations.

Methods
Developmental rate data – collected by daily monitoring of larval development (naupliar and copepodid) of individual Tigriopus californicus until either stage 1 copepodid metamorphosis was observed or adulthood was reached.

ATP synthesis rate data – mitochondria isolated by differential centrifugation followed by in vitro assays of maximal ATP synthesis rate with saturating concentrations of substrates for either electron transport complex I or II.

种群内协同演化的遗传互作可因杂交而被破坏，进而导致杂交个体的适合度下降（即杂交衰退（hybrid breakdown））。然而，杂交后代中适合度相关性状的变异在跨世代间的遗传程度仍不明确；且由于雌雄个体间遗传不相容性的作用存在差异，这类性状的变异在杂交后代中可能具有性别特异性。本研究针对潮间带桡足类虎斑猛水蚤（Tigriopus californicus）的种群间互交杂交后代的发育速率变异开展了两项实验。在该物种中，发育速率是一项与适合度相关的性状，其会受到杂交后代中线粒体编码基因与核编码基因之间互作的影响，这种互作会导致线粒体ATP合成能力产生变异。其一，两项互交组合的F₂代杂交后代发育速率并无差异，且不受性别影响，这表明发育速率衰退在雌雄个体间的发生程度可能相当。其二，F₃代杂交后代的发育速率变异具有可遗传性：发育较快的F₃亲本所产生的F₄后代，其桡足幼体变态所需时间为12.25±0.05天（均值±标准误），显著快于发育较慢的F₃亲本所产生的F₄后代（14.58±0.05天）。其三，本研究发现，这些F₄代杂交后代的ATP合成速率不受其亲本发育速率的影响，但雌性个体的线粒体合成ATP的速率显著快于雄性个体的线粒体。综合来看，这些结果表明，在这类杂交后代中，适合度相关性状的性别特异性效应存在差异，且与杂交衰退相关的效应在杂交世代间具有显著的可遗传性。

材料与方法
发育速率数据：通过每日监测单只虎斑猛水蚤（Tigriopus californicus）的幼体发育阶段（无节幼体与桡足幼体），直至观察到第1期桡足幼体变态或个体发育至成虫。
ATP合成速率数据：通过差速离心法分离线粒体，随后以电子传递复合体I或II的饱和浓度底物进行体外实验，测定最大ATP合成速率。