Multiple mating, paternity and complex fertilisation patterns in the chokka squid Loligo reynaudi

Polyandry is widespread and influences patterns of sexual selection, with implications for sexual conflict over mating. Assessing sperm precedence patterns is a first step towards understanding sperm competition within a female and elucidating the roles of male- and female-controlled factors. In this study behavioural field data and genetic data were combined to investigate polyandry in the chokka squid Loligo reynaudii. Microsatellite DNA-based paternity analysis revealed multiple paternity to be the norm, with 79% of broods sired by at least two males. Genetic data also determined that the male who was guarding the female at the moment of sampling was a sire in 81% of the families tested, highlighting mate guarding as a successful male tactic with postcopulatory benefits linked to sperm deposition site giving privileged access to extruded egg strings. As females lay multiple eggs in capsules (egg strings) wherein their position is not altered during maturation it is possible to describe the spatial / temporal sequence of fertilisation / sperm precedence There were four different patterns of fertilisation found among the tested egg strings: 1) unique sire; 2) dominant sire, with one or more rare sires; 3) randomly mixed paternity (two or more sires); and 4) a distinct switch in paternity occurring along the egg string. The latter pattern cannot be explained by a random use of stored sperm, and suggests postcopulatory female sperm choice. Collectively the data indicate multiple levels of male- and female-controlled influences on sperm precedence, and highlights squid as interesting models to study the interplay between sexual and natural selection.

一妻多夫制（Polyandry）分布广泛，可影响性选择（sexual selection）模式，对交配过程中的性冲突（sexual conflict）具有重要意义。解析精子优先（sperm precedence）模式，是阐明雌性体内精子竞争（sperm competition）机制、阐明雌雄双方调控因子作用的首要步骤。本研究整合野外行为学数据与遗传学数据，对莱氏枪乌贼（Loligo reynaudii，chokka squid）的一妻多夫制展开探究。基于微卫星DNA（microsatellite DNA）的父权（paternity）分析结果显示，多父本现象（multiple paternity）为常态：79%的幼群（broods）至少由两只雄性授精。遗传学数据同时证实，在81%的受测家系中，采样时正守护雌性的雄性即为父本（sire）之一，这表明护偶行为（mate guarding）是一种成功的雄性繁殖策略——其交配后收益（postcopulatory benefits）与精子沉积位点（sperm deposition site）相关，可使该雄性优先接触排出的卵索（egg strings）。由于雌性会将多枚卵产于卵囊（capsule）中，该结构亦被称为卵索（egg strings），且卵在成熟过程中位置不会发生改变，因此可解析受精/精子优先模式的空间与时间序列。受测卵索中共存在四种不同的受精模式：1）单一父本；2）优势父本伴随1个或多个稀有父本；3）父本随机混合（含2个及以上父本）；4）卵索上出现显著的父本类型转换。第四种模式无法通过精子的随机利用来解释，这表明雌性存在交配后的精子选择（sperm choice）行为。综合来看，本研究数据表明，雌雄双方在多个层面上对精子优先模式存在调控影响，同时也凸显出枪乌贼是探究性选择与自然选择间相互作用的优质实验模型。