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The evolution of community assembly in marine foundation species
Functional Ecology ( IF 5.2 ) Pub Date : 2020-10-07 , DOI: 10.1111/1365-2435.13659
Rebecca J. Best 1
Affiliation  

Community diversity controls ecosystem function, but the supply and replacement of that diversity is ultimately controlled by evolution. Integrating community processes with evolutionary opportunity is therefore central to understanding the future of biodiversity in a changing world. Losos (1996) pointed this out over two decades ago when he showed that we cannot infer mechanisms of community assembly and coexistence without accounting for the evolutionary history constraining the pool of species available to be assembled. There was already evidence that regional species richness could constrain community species richness (Cornell & Harrison, 2014; Cornell & Lawton, 1992; Ricklefs, 1987), but Losos’ point spurred new interest in thinking about evolutionary constraints on species’ traits in relation to community assembly. Using the assumption of niche conservatism, a community phylogeny could be used to account for evolution and provide a proxy for ecological similarity among species (Webb, Ackerly, McPeek, & Donoghue, 2002). This resulted in an explosion of tests of whether communities are composed of closely related species similarly filtered by the environment, or distantly related species avoiding competitive exclusion by using different resources. However, in systems where much of the community being assembled is drawn from a single lineage that lends itself to careful understanding of trait evolution, it was soon clear that species like oaks (Cavender‐Bares, 2019) and anoles (Losos et al., 2003) could evolve convergently to fill available niches. Thus, close relatives cannot be assumed to be the most similar in any particular trait. Furthermore, the failure of close relatives to co‐occur locally could simply be the expected signature of allopatric speciation (Pigot & Etienne, 2015; Warren, Cardillo, Rosauer, & Bolnick, 2014) or recent divergence in micro‐habitats (Anacker & Strauss, 2014).

So how do we better integrate evolution with community ecology, given this complexity? One major answer is the idea of a ‘model lineage’ (Cavender‐Bares, 2019), where assembling both evolutionary and ecological information about an important group of relatives (like oaks) lets us accurately test questions about the interplay of diversification and coexistence. In this issue of Functional Ecology, Starko and Martone (2020) present the evolution and ecology of kelps (a group of large marine brown algae), providing an excellent first example of a marine ‘model lineage’. These authors have traced the diversification of kelps through the evolutionary opportunities of the last 30 million years (Starko et al., 2019) and into the composition of contemporary communities on the eastern Pacific coast (Starko & Martone, 2020). Unlike many marine systems composed of invertebrates from deeply diverged phyla, where important interactions between very distant relatives make it difficult to test community interactions in an evolutionary framework (Wilcox, Schwartz, & Lowe, 2018), kelps have excellent potential as a model lineage for the ocean. The relatively recent history of diversification in this system is much more likely to be influenced by the same selection pressures and environmental gradients relevant for communities observed today, offering important opportunities to do truly integrative work on how species interactions alter evolution (Weber, Wagner, Best, Harmon, & Matthews, 2017) and how evolution shapes species interactions (Cavender‐Bares, Kozak, Fine, & Kembel, 2009; Gerhold, Cahill, Winter, Bartish, & Prinzing, 2015; Haloin & Strauss, 2008).

Using traits, a phylogeny and community data, Starko and Martone (2020) show that kelp species are filtered by their wave tolerance into communities along a wave exposure gradient. Using specific traits with known functional consequences (Starko & Martone, 2016) strengthens this conclusion relative to analyses of general similarity in community members (Kraft et al., 2015). Then, using ancestral trait reconstructions and tests for phylogenetic signal (the correspondence between time for divergence and actual divergence in traits), the authors show that these wave tolerance traits have evolved convergently across the kelp phylogeny. This convergent evolution is shaped by clear morphological trade‐offs, which are central to understanding the evolution of niche specialization in any system (Poisot, Bever, Nemri, Thrall, & Hochberg, 2011). Kelps can adapt to deal with (a) the stress of higher flow and potential dislodgement, either by streamlining their morphology or by investing more energy in the holdfast (Starko & Martone, 2016), or (b) with the stress of still water and boundary layers that make the uptake of CO2 and nutrients more difficult (Starko, Claman, & Martone, 2015). As with oaks (Cavender‐Bares, Ackerly, Baum, & Bazzaz, 2004), repeated evolution of these strategies across the phylogeny results in the co‐occurrence of distant relatives in locations with the same stressors.

As we start to assemble a broader range of ‘model lineages’ across ecosystems, we can better ask questions about the general rates and constraints of evolution to fill environmental (beta) versus local (alpha) niches. In the few examples starting to accumulate, traits related to environmental tolerances can be more conserved (Ackerly, Schwilk, & Webb, 2006; Silvertown, Dodd, Gowing, Lawson, & McConway, 2006), or less conserved (Cavender‐Bares et al., 2004; Emery et al., 2012) than those related to local resource partitioning. This results in the occupancy of stressful habitats either by a few close relatives that can tolerate conditions (Best & Stachowicz, 2014; Kembel & Hubbell, 2006) or convergent specialists from many branches of the phylogeny (Savage & Cavender‐Bares, 2012). In kelps, the repeated evolution of wave tolerance could have been facilitated by the availability of wave‐swept niches at the time of their radiation (Fukami, 2015; Tanentzap et al., 2015), or patterns of dispersal (Verbruggen et al., 2009), or the relative physiological flexibility of specific traits needed for withstanding wave stress versus accessing light locally available in a multi‐species assemblage. Having a greater diversity of systems to test these hypotheses is important because it should help us predict how evolution might contribute new biodiversity to fill new environmental niches opened by anthropogenic change.

In addition to their interesting evolutionary history, kelps also serve an important role as exclusive providers of really three‐dimensional marine forest habitat, feeding herbivores and mediating trophic interactions (Steneck et al., 2002). This means that a single lineage captures the full community of foundation species even more so than oaks, which interact with other angiosperms and gymnosperms (Cavender‐Bares, Keen, & Miles, 2006). A model lineage in this context offers some very interesting opportunities to explore evolutionary interactions between kelps and invertebrate herbivores, which have preferences for different kelp morphologies as habitat (Stelling‐Wood, Gribben, & Poore, 2020) and food (Rhoades, Best, & Stachowicz, 2018) and in turn impact producer performance (Poore et al., 2012). Given that kelps exhibit evolutionary trade‐offs between fast growth and defended growth that in some ways parallel those in terrestrial plants (Starko & Marone, 2020), there is great potential for the study of co‐diversification across trophic levels in kelp‐associated systems, as well as the consequences of ecosystem evolution for ecosystem function (Srivastava, Cadotte, MacDonald, Marushia, & Mirotchnick, 2012). Whether we are interested in the future links between diversity and ecosystem health, or in making more accurate conclusions about the forces shaping coexistence versus extirpation today, systems offering integrated insight about the sources and consequences of biodiversity are extremely valuable.



中文翻译:

海洋基础物种群落组装的演变

社区多样性控制着生态系统的功能,但是这种多样性的供应和替代最终受进化的控制。因此,将社区过程与进化机会相结合对于理解变化中的世界中生物多样性的未来至关重要。Losos(1996)在二十多年前就指出了这一点,当时他表明如果不考虑进化史限制了可聚集物种的种群,我们就无法推断出社区聚集和共存的机制。已经有证据表明区域物种丰富度可能会限制社区物种丰富度(Cornell&Harrison,  2014 ; Cornell&Lawton,  1992 ; Ricklefs,  1987)),但Losos的观点激发了人们对与社区聚集有关的物种特征进化限制的思考的新兴趣。使用利基保守性的假设,可以将群落系统发育用于解释进化,并为物种之间的生态相似性提供代理(Webb,Ackerly,McPeek和Donoghue,  2002年)。这导致了测试的爆炸式增长,即社区是由环境相似过滤的紧密相关物种组成,还是由远距离相关的物种通过使用不同的资源避免竞争排斥而组成的。然而,在许多社区的聚集都是从单一血统中抽取出来的系统中,这有助于仔细了解特质的进化,很快就知道了像橡树这样的物种(Cavender-Bares,  2019)和anoles(Losos et al。,2003)可能会不断演化,以填补可用的生态位。因此,不能认为近亲在任何特定特征上都是最相似的。此外,近亲未能在当地共同生活可能只是异特异物种形成的预期特征(Pigot和Etienne,  2015年; Warren,Cardillo,Rosauer和Bolnick,  2014年)或近期在小生境上的分歧(Anacker和Strauss) ,  2014年)。

那么,鉴于这种复杂性,我们如何更好地将进化与社区生态整合在一起?一个主要的答案是``模型谱系''的想法(Cavender-Bares,  2019年),其中汇集了关于重要亲戚(如橡树)的进化和生态信息,使我们能够准确地测试关于多样化和共存相互作用的问题。在本期《功能生态学》中,Starko和Martone(2020)介绍了海带(一组大型海洋褐藻)的演化和生态学,为海洋“模型谱系”提供了一个极好的示例。这些作者通过过去三千万年的进化机会追溯了海带的多样化(Starko等人,  2019),并将其纳入东太平洋沿岸的当代社区构成(Starko和Martone,  2020年)。与许多由深散无脊椎动物的无脊椎动物组成的海洋系统不同,非常遥远的亲戚之间的重要相互作用使得很难在进化框架中测试群落相互作用(Wilcox,Schwartz,&Lowe,  2018),海带具有极好的潜力,可以作为海藻的模型世系海洋。该系统中相对较新的多样化历史很可能受到与今天所观察到的社区相关的相同选择压力和环境梯度的影响,这为开展真正的整合工作以研究物种相互作用如何改变进化提供了重要的机会(Weber,Wagner,Best ,Harmon和Matthews,  2017年)以及进化如何影响物种之间的相互作用(Cavender-Bares,Kozak,Fine和Kembel,  2009年; Gerhold,Cahill,Winter,Bartish和Prinzing,  2015年; Haloin和Strauss,  2008年)。

利用性状,系统发育和群落数据,Starko和Martone(2020)表明,海藻物种通过其波耐受性被滤过,并沿着波暴露梯度进入群落。相对于对社区成员普遍相似性的分析(Kraft et al。,2015),使用具有已知功能后果的特定性状(Starko&Martone,  2016)可以加强这一结论。 )。然后,使用祖先特征重建和系统发育信号测试(特征发散时间与实际发散时间之间的对应关系),作者表明,这些耐波性状在整个海带系统发育中均趋于融合。这种趋同的演化是由清晰的形态权衡决定的,这是理解任何系统中利基专业化发展的关键(Poisot,Bever,Nemri,Thall和Hochberg,  2011年)。海带可以通过以下方式适应处理(a)较高流量和潜在移位的压力,方法是精简其形态或在固定装置中投入更多的能量(Starko和Martone,  2016年),或(b)承受静水压力和吸收CO 2的边界层和营养更困难(Starko,Claman和Martone,  2015年)。与橡木一样(Cavender-Bares,Ackerly,Baum和Bazzaz,  2004年),这些策略在系统发生上的反复演变导致远亲在同一个压力源下同时出现。

随着我们开始在整个生态系统中收集更广泛的“模型谱系”,我们可以更好地提出有关填充环境(β)和局部(α)生态位的总体速率和约束条件的问题。在开始积累的几个例子中,与环境耐受性相关的特征可以更保守(Ackerly,Schwilk和Webb,  2006; Silvertown,Dodd,Gowing,Lawson和McConway,  2006),或者不那么保守(Cavender-Bares等人) (  2004年; Emery等人,  2012年)。这导致一些可以忍受条件的近亲占据压力大的栖息地(Best和Stachowicz,  2014年; Kembel和Hubbell,  2006年)。)或来自系统发育许多分支的专家(Savage&Cavender-Bares,  2012年)。在海带中,辐射波辐射的壁ni在辐射时的可用性(Fukami,  2015 ; Tanentzap et al。,  2015)或扩散方式(Verbruggen et al。,  2009),或抵御波浪胁迫与获取多物种组合中本地可用的光所需的特定性状的相对生理灵活性。有更多的系统多样性来检验这些假设很重要,因为它可以帮助我们预测进化将如何贡献新的生物多样性,以填补人为变化所带来的新的环境壁ni。

除了其有趣的进化史外,海带还作为真正的三维海洋森林生境,提供食草动物和介导营养相互作用的独家提供者(Steneck等,  2002)。这意味着,一个单一的宗族比起与其他被子植物和裸子植物相互作用的橡树更能捕获整个基础物种群落(Cavender-Bares,Keen,&Miles,  2006)。在此背景下的模型谱系为探索海带和无脊椎动物草食动物之间的进化相互作用提供了一些非常有趣的机会,它们对生境(Stelling-Wood,Gribben和Poore,  2020年)和食物(Rhoades,Best和&斯塔乔维奇,  2018),进而影响生产者的绩效(Poore等,2012)。鉴于海带表现出快速增长与防御性增长之间的进化权衡,在某种程度上与陆地植物相似(Starko&Marone,2020年),因此研究海带相关系统中营养水平上的共生多样性具有巨大潜力。以及生态系统演化对生态系统功能的影响(Srivastava,Cadotte,MacDonald,Marushia和Mirotchnick,  2012年)。无论是我们对多样性与生态系统健康之间的未来联系感兴趣,还是对当今影响共存与灭绝的力量做出更准确的结论,提供有关生物多样性的来源和后果的综合见解的系统都非常有价值。

更新日期:2020-10-07
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