Hewitt Trevor L, Haponski Amanda E, Foighil Diarmaid Ó
Department of Ecology and Evolutionary Biology and Museum of Zoology, University of Michigan - Ann Arbor, Ann Arbor, MI, United States of America.
PeerJ. 2021 Nov 16;9:e12287. doi: 10.7717/peerj.12287. eCollection 2021.
North American watersheds contain a high diversity of freshwater mussels (Unionoida). During the long-lived, benthic phase of their life cycle, up to 40 species can co-occur in a single riffle and there is typically little evidence for major differences in their feeding ecology or microhabitat partitioning. In contrast, their brief parasitic larval phase involves the infection of a wide diversity of fish hosts and female mussels have evolved a spectrum of adaptations for infecting host fish with their offspring. Many species use a passive broadcast strategy: placing high numbers of larvae in the water column and relying on chance encounters with potential hosts. Many other species, including most members of the Lampsilini, have a proactive strategy that entails the use of prey-mimetic lures to change the behavior of the hosts, , eliciting a feeding response through which they become infected. Two main lure types are collectively produced: mantle tissue lures (on the female's body) and brood lures, containing infective larvae, that are released into the external environment. In this study, we used a phylogenomic approach (ddRAD-seq) to place the diversity of infection strategies used by 54 North American lampsiline mussels into an evolutionary context. Ancestral state reconstruction recovered evidence for the early evolution of mantle lures in this clade, with brood lures and broadcast infection strategies both being independently derived twice. The most common infection strategy, occurring in our largest ingroup clade, is a mixed one in which mimetic mantle lures are apparently the predominant infection mechanism, but gravid females also release simple, non-mimetic brood lures at the end of the season. This mixed infection strategy clade shows some evidence of an increase in diversification rate and most members use centrarchids ( & spp.) as their predominant fish hosts. Broad linkage between infection strategies and predominant fish host genera is also seen in other lampsiline clades: worm-like mantle lures of spp. with sunfish ( spp.); insect larvae-like brood lures ( spp.), or mantle lures ( spp., spp.), or mantle lures combined with host capture ( spp.) with a spectrum of darter ( & spp.) and sculpin ( spp.) hosts, and tethered brood lures ( spp.) with bass ( spp.). Our phylogenetic results confirm that discrete lampsiline mussel clades exhibit considerable specialization in the primary fish host clades their larvae parasitize, and in the host infection strategies they employ to do so. They are also consistent with the hypothesis that larval resource partitioning of fish hosts is an important factor in maintaining species diversity in mussel assemblages. We conclude that, taking their larval ecology and host-infection mechanisms into account, lampsiline mussels may be legitimately viewed as an adaptive radiation.
北美流域拥有高度多样化的淡水贻贝(蚌目)。在其生命周期中漫长的底栖阶段,多达40个物种可在同一浅滩共同出现,而且通常几乎没有证据表明它们在摄食生态或微生境划分上存在重大差异。相比之下,它们短暂的寄生幼虫阶段涉及感染多种鱼类宿主,并且雌性贻贝已经进化出一系列适应方式,以便用其后代感染宿主鱼类。许多物种采用被动散播策略:将大量幼虫释放到水柱中,依靠与潜在宿主的偶然相遇。许多其他物种,包括大多数灯蚌科成员,具有主动策略,即利用拟饵来改变宿主的行为,引发摄食反应从而使它们被感染。总共产生两种主要的拟饵类型:外套膜组织拟饵(在雌性身体上)和含有感染性幼虫的育幼拟饵,育幼拟饵会被释放到外部环境中。在本研究中,我们采用了一种系统基因组学方法(ddRAD测序),将54种北美灯蚌科贻贝所采用的感染策略的多样性置于进化背景中。祖先状态重建恢复了该类群中外套膜拟饵早期进化的证据,育幼拟饵和散播感染策略均独立起源了两次。最常见的感染策略出现在我们最大的内类群分支中,是一种混合策略,其中拟态外套膜拟饵显然是主要的感染机制,但怀有身孕的雌性在季节末期也会释放简单的、非拟态的育幼拟饵。这个混合感染策略分支显示出一些多样化速率增加的证据,并且大多数成员以太阳鱼科(太阳鱼属和丽鱼属物种)作为其主要的鱼类宿主。在其他灯蚌科分支中也可以看到感染策略与主要鱼类宿主属之间的广泛联系:眼点蚌属物种的蠕虫状外套膜拟饵与翻车鱼(翻车鲀属物种);似昆虫幼虫的育幼拟饵(隐瘤蚌属物种),或外套膜拟饵(石蚌属物种、褶纹冠蚌属物种),或与捕获宿主相结合的外套膜拟饵(石蛏属物种)与一系列镖鲈(镖鲈属和美洲鲈属物种)和杜父鱼(杜父鱼属物种)宿主,以及带有系绳的育幼拟饵(球蚌属物种)与鲈鱼(鲈属物种)。我们的系统发育结果证实,不同的灯蚌科贻贝分支在其幼虫寄生的主要鱼类宿主分支以及它们所采用的宿主感染策略方面表现出相当程度的特化。它们也与以下假设一致,即鱼类宿主的幼虫资源划分是维持贻贝群落物种多样性的一个重要因素。我们得出结论,考虑到它们的幼虫生态学和宿主感染机制,灯蚌科贻贝可以被合理地视为一次适应性辐射。