Temperature stress induces mites to help their carrion beetle hosts by eliminating rival blowflies

Ecological conditions are known to change the expression of mutualisms though the causal agents driving such changes remain poorly understood. Here we show that temperature stress modulates the harm threatened by a common enemy, and thereby induces a phoretic mite to become a protective mutualist. Our experiments focus on the interactions between the burying beetle Nicrophorus vespilloides, an associated mite species Poecilochirus carabi and their common enemy, blowflies, when all three species reproduce on the same small vertebrate carrion. We show that mites compete with beetle larvae for food in the absence of blowflies, and reduce beetle reproductive success. However, when blowflies breed on the carrion too, mites enhance beetle reproductive success by eating blowfly eggs. High densities of mites are especially effective at promoting beetle reproductive success at higher and lower natural ranges in temperature, when blowfly larvae are more potent rivals for the limited resources on the carcass

Conflict within species determines the value of a mutualism between species.

Mutually beneficial interactions between species play a key role in maintaining biodiversity and ecosystem function. Nevertheless, such mutualisms can erode into antagonistic interactions. One explanation is that the fitness costs and benefits of interacting with a partner species vary among individuals. However, it is unclear why such variation exists. Here, we demonstrate that social behavior within species plays an important, though hitherto overlooked, role in determining the relative fitness to be gained from interacting with a second species. By combining laboratory experiments with field observations, we report that conflict within burying beetles Nicrophorus vespilloides influences the fitness that can be gained from interacting with the mite Poecilochirus carabi. Beetles transport these mites to carrion, upon which both species breed. We show that mites help beetles win intraspecific contests for this scarce resource: mites raise beetle body temperature, which enhances beetle competitive prowess. However, mites confer this benefit only upon smaller beetles, which are otherwise condemned by their size to lose contests for carrion. Larger beetles need no assistance to win a carcass and then lose reproductive success when breeding alongside mites. Thus, the extent of mutualism is dependent on an individual's inability to compete successfully and singlehandedly with conspecifics. Mutualisms degrade into antagonism when interactions with a partner species start to yield a net fitness loss, rather than a net fitness gain. This study suggests that interactions with conspecifics determine where this tipping point lies

Climate-mediated cooperation promotes niche expansion in burying beetles

The ability to form cooperative societies may explain why humans and social insects have come to dominate the earth. Here we examine the ecological consequences of cooperation by quantifying the fitness of cooperative (large groups) and non-cooperative (small groups) phenotypes in burying beetles (Nicrophorus nepalensis) along an elevational and temperature gradient. We experimentally created large and small groups along the gradient and manipulated interspecific competition with flies by heating carcasses. We show that cooperative groups performed as thermal generalists with similarly high breeding success at all temperatures and elevations, whereas non-cooperative groups performed as thermal specialists with higher breeding success only at intermediate temperatures and elevations. Studying the ecological consequences of cooperation may not only help us to understand why so many species of social insects have conquered the earth, but also to determine how climate change will affect the success of these and other social species, including our own

Temperature stress induces mites to help their carrion beetle hosts by eliminating rival blowflies

Ecological conditions are known to change the expression of mutualisms though the causal agents driving such changes remain poorly understood. Here we show that temperature stress modulates the harm threatened by a common enemy, and thereby induces a phoretic mite to become a protective mutualist. Our experiments focus on the interactions between the burying beetle Nicrophorus vespilloides, an associated mite species Poecilochirus carabi and their common enemy, blowflies, when all three species reproduce on the same small vertebrate carrion. We show that mites compete with beetle larvae for food in the absence of blowflies, and reduce beetle reproductive success. However, when blowflies breed on the carrion too, mites enhance beetle reproductive success by eating blowfly eggs. High densities of mites are especially effective at promoting beetle reproductive success at higher and lower natural ranges in temperature, when blowfly larvae are more potent rivals for the limited resources on the carcass.Taiwan Cambridge Scholarship Cambridge Commonwealth, European and International Trust European Research Council Grant 301785 BALDWINIAN_BEETLES Wolfson Merit Award from the Royal Societ

On the ecological transitions between parasitism and mutualism

Species interactions are pivotal to biodiversity structure and ecosystem functioning. Nevertheless, interactions between species are ecologically variable within the same pair of interacting species, lying on a mutualism-parasitism continuum. Identifying the underlying mechanisms and context dependency of such ecological dynamics is essential to understand the responses of interacting species to rapidly changing environments. In this thesis, I investigate the ecological factors that cause transitions between parasitism and mutualism, using the burying beetles (Nicrophorus vespilloides) and their phoretic mites (the species complex Poecilochirus carabi) as a model symbiosis. I begin by showing that P. carabi is the most abundant mite species associating with burying beetles, and that it coexists with the mite Macrocheles nataliae. I show that each species attaches to a distinct part of the beetle’s body, so facilitating their co-existence. Furthermore, I show that distinct behavioural and biomechanical adaptations enable each mite species to occupy their preferred locations. This finding reveals that niche partitioning can occur within macroscopic symbiotic communities even when they coexist upon the same host animal. Next, I investigate whether P. carabi mites and N. vespilloides are ever (by-product) mutualists. I assess whether mites assist beetles when competing with conspecifics for ownership of the carcass. Using infrared thermography, I find that beetles with mites attain a higher body temperature, and that this makes them more likely to win contests against conspecifics. However, mites confer this thermal benefit only upon smaller beetles, who generate more heat than larger beetles when carrying mites, which is then trapped by the layer of mites on the beetle’s body. For larger beetles, mites are parasitic. They maintain a high body temperature and win contests for a carcass singlehandedly, and then produce fewer larvae when breeding alongside mites. Burying beetles also commonly face fierce competition from blowflies for the resources upon a carcass. Combining field manipulations and laboratory experiments, I find that mites are in a protective mutualism with beetles because they eliminate blowflies from the carcass, and so promote burying beetle reproductive success. I also find that the extent of this mutualism is dependent upon temperature. At lower temperatures, and when blowflies are absent, mites reduce beetle reproductive success. They are most effective at promoting beetle reproductive success at higher temperatures, at which blowflies pose more of a competitive threat. Finally, I investigate whether the number of burying beetle species present in a woodland can tip the relationship between mites and their N. vespilloides hosts from mutualism to parasitism. I discover that neighbouring woodlands (Waresley and Gamlingay Woods in Cambridgeshire, UK) harbour two and four species of burying beetle, respectively. Furthermore, each species of burying beetle is associated with a different race of P. carabi mite. I show that mite races can be locally adapted to their host beetle species. However, I also find that mite races mix, so that one burying beetle species can be host to multiple P. carabi mite races, and that this happens more frequently when there are more burying beetle species present in one woodland. Burying beetles are then more likely to be in an antagonistic relationship with the mites they carry: local adaptation experiments reveal that N. vespilloides in Gamlingay Wood is in a more antagonistic relationship with P. carabi mites than N. vespilloides from Waresley Wood. Thus temperature, the density of mites and the density of rivals for the carrion breeding resource independently influence whether the relationship between N. vespilloides and P. carabi is more likely to be mutualistic or antagonistic.Taiwan Cambridge Scholarship (The Cambridge Commonwealth, European & International Trust

Competition among host‐specific lineages of <i>Poecilochirus carabi</i> mites influences the extent of co‐adaptation with their <i>Nicrophorus vespilloides</i> burying beetle hosts

Publication status: PublishedFunder: National Taiwan University; doi: http://dx.doi.org/10.13039/501100006477Funder: Cambridge Commonwealth, European & International Trust; doi: http://dx.doi.org/10.13039/501100003343Funder: Royal Society; doi: http://dx.doi.org/10.13039/501100000288Funder: Ministry of Education, TaiwanAbstractReciprocal selection between symbiotic organisms and their hosts can generate variations in local adaptation between them. Symbionts often form species complexes with lineages partially adapted to various hosts. However, it is unclear how interactions among these lineages influences geographic variation in the extent of host‐symbiont local adaptation. We addressed this shortcoming with experiments on burying beetles Nicrophorus vespilloides and their specialist phoretic mite Poecilochirus carabi in two adjacent woodlands. Burying beetles transport these mites to vertebrate carrion upon which they both reproduce. P. carabi appears to be a species complex, with distinct lineages that specialise on breeding alongside different Nicrophorus species. We found that in one wood (Gamlingay Woods), N. vespilloides carries a mixture of mite lineages, with each lineage corresponding to one of the four Nicrophorus species that inhabits this wood. However, two burying beetle species coexist in neighbouring Waresley Woods and here N. vespilloides predominantly carries the mite lineage that favours N. vespilloides. Mite lineage mixing alters the degree of local adaptation for both N. vespilloides and the P. carabi mites, affecting reproductive success variably across different woodlands. In Gamlingay, mite lineage mixing reduced N. vespilloides reproductive success, while experimentally purifying mites lineage enhanced it. The near pure lineage of vespilloides mites negligibly affected Waresley N. vespilloides. Mite reproductive success varied with host specificity: Gamlingay mites had greatest reproductive success on Gamlingay beetles, and performed less well with Waresley beetles. By contrast, Waresley mites had consistent reproductive success, regardless of beetle's woodland of origin. We conclude that there is some evidence that N. vespilloides and its specific mite lineage have coadapted. However, neither N. vespilloides nor its mite lineage adapted to breed alongside other mite lineages. This, we suggest, causes variation between Waresley and Gaminglay Woods in the extent of local adaptation between N. vespilloides beetles and their P. carabi mites.</jats:p

Digest: Deprivation of parental care reveals the value of sibling cooperation in burying beetles

What conditions favor cooperation in sibling interactions? In burying beetles of the genus Nicrophorus, Prang et al. found that dependence on parental care cannot solely explain the degree of offspring cooperation. While only larvae of independent species cooperated when receiving pre‐hatching care, both independent and dependent species cooperated in the absence of pre‐hatching care. This finding suggests that offspring cooperation has persisted from an early ancestor of the genus Nicrophorus to the present species, highlighting the evolution from facultative to obligatory social behavior.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/172083/1/evo14451_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/172083/2/evo14451.pd

Climate-mediated Cooperation Promotes Niche Expansion in Burying Beetles (Nicrophorus nepalensis Hope 1831)

長久以來，科學家試圖解開人類與社會性生物適應各種陸域棲地的原因，其中一項可能的解釋為──合作行為促使人類與社會性生物成為生態上的優勢種，而佔據各種不同的生態棲位。尼泊爾埋葬蟲廣泛分佈於台灣的中海拔山區，以小群體的合作方式利用動物屍體為繁殖資源。由於利用屍體的昆蟲繁多，搶奪屍體激烈，因此埋葬蟲在異種競爭劇烈的環境會採取合作生殖的策略。本研究重要的發現為：第一，直接證明溫度梯度改變物種間的競爭角力。第二，直接證明合作行為對物種的競爭力有正面的影響，幫助物種棲位向外擴張。本研究以具有合作生殖特性的尼泊爾埋葬蟲 (Nicrophorus nepalensis) 做為實驗物種，沿著海拔梯度進行大尺度操縱性實驗，在自然條件下創造大群體與小群體的埋葬蟲，以操控社會性與非社會性的群體。此外，本研究也以加熱實驗增強蠅類分解屍體的競爭力，探究埋葬蟲合作生殖對抗種間競爭的生態結果。結果顯示大群體埋葬蟲沿著海拔與溫度梯度均有較高且穩定的繁殖成功率，而小群體埋葬蟲則只在中海拔有較高的繁殖成功率。在低海拔氣溫較高且種間競爭較強的環境，大群體埋葬蟲合作處理屍體的投資時間增加，也因此具有較高的繁殖成功率。實驗結果進一步顯示加熱屍體能增強蠅類的競爭力，減低小群體的繁殖成功率，而大群體卻能透過合作對抗蠅類的種間競爭。由此可知，小群體和狹適性物種相仿，而大群體埋葬蟲沿海拔與溫度梯度的繁殖表現則近似廣適性物種，透過合作促進生態棲位寬度擴張。透過瞭解合作行為的生態結果，本研究不但解釋了為什麼社會昆蟲能征服陸域生態系，也有助於瞭解氣候變遷如何影響人類與其他社會性生物的行為生存策略。The ability to form cooperative societies may explain why humans and social insects have come to dominate the earth. Here we examine the ecological consequences of cooperation by quantifying the fitness of cooperative (large groups) and non-cooperative (small groups) phenotypes in burying beetles (Nicrophorus nepalensis) along an elevational and temperature gradient. We experimentally created large and small groups along the gradient and manipulated interspecific competition with flies by heating carcasses. We show that cooperative groups performed as thermal generalists with similarly high breeding success at all temperatures and elevations, whereas non-cooperative groups performed as thermal specialists with higher breeding success only at intermediate temperatures and elevations. Studying the ecological consequences of cooperation may not only help us to understand why so many species of social insects have conquered the earth, but also to determine how climate change will affect the success of these and other social species, including our own.目錄 口試委員會審定書 I 誌謝 II 中文摘要 IV ABSTRACT V 目錄 VI 圖目錄 VIII 表目錄 IX CHAPTER 1 前言 1 CHAPTER 2 材料與方法 5 2.1 研究物種 5 2.2 自然環境下蠅類競爭力與尼泊爾埋葬蟲的表現 5 2.2.1 實驗樣區 5 2.2.2 屍食性昆蟲在大鼠屍體上的演替 6 2.2.3 尼泊爾埋葬蟲的群大小與繁殖成功率 6 2.3 不同環境下社會性對尼泊爾埋葬蟲的影響 7 2.3.1 尼泊爾埋葬蟲的採集 7 2.3.2 群體大小的操控 7 2.3.3 不同環境下蠅類的競爭強度 9 2.3.4 加熱屍體以操控蠅類的競爭強度 9 2.4 行為分析 9 2.5 統計分析 10 CHAPTER 3 研究結果 12 3.1 自然狀況下埋葬蟲的群大小與群體繁殖表現 12 3.2 尼泊爾埋葬蟲合作行為對生態棲位寬度的影響 12 3.3 尼泊爾埋葬蟲在不同環境下的合作與衝突 13 3.4 蠅類的種間競爭對尼泊爾埋葬蟲繁殖表現的影響 14 3.4.1 屍食性昆蟲在大鼠屍體上的演替 14 3.4.2 不同環境下蠅類的競爭強度 14 3.4.3 加熱屍體以操控蠅類的競爭強度 15 CHAPTER 4 討論 16 4.1 生態因子對埋葬蟲合作生殖演化的影響 16 4.2 合作行為促使尼泊爾埋葬蟲生態棲位擴張 17 4.3 未來研究方向 18 CHAPTER 5 結論 19 參考文獻 20 附錄一：期刊發表 42 附錄二：相關報導 63 圖目錄 圖 一、生物社會性形成的原因及其對生態棲位寬度的影響 23 圖 二、瑞岩溪自然保護區環境概況 24 圖 三、陷阱裝置圖 25 圖 四、臺灣南投縣實驗樣區沿海拔的空間分布 (24°5’ N, 121°10’ E ) 26 圖 五、自然狀況下埋葬蟲群大小與繁殖成功率沿環境梯度的變化 27 圖 六、自然狀況下埋葬蟲群體總投資 (單位：分鐘) 隨群大小的變化 28 圖 七、群體大小操控實驗陷阱裝置圖 29 圖 八、操縱性實驗控制大群體與小群體埋葬蟲的平均群大小 30 圖 九、大群體與小群體埋葬蟲繁殖成功率沿環境梯度的變化 31 圖 十、大群體與小群體埋葬蟲總投資時間沿環境梯度的變化 32 圖 十一、屍體完全消耗所需天數沿海拔梯度的變化 33 圖 十二、加熱組與控制組中蠅類豐富度與日間活動力沿環境梯度的變化 34 圖 十三、大群體與小群體平均每隻埋葬蟲社會衝突沿環境梯度的變化 35 圖 十四、蠅類種間競爭對屍體重量消耗的影響 36 圖 十五、自然狀況下蠅類競爭對埋葬蟲繁殖成功率的影響 37 圖 十六、加熱屍體對大群體與小群體埋葬蟲繁殖成功率與總投資時間的影響 38 表目錄 表 一、大鼠屍體演替前期各屍食性昆蟲的豐富度與科別鑑定 39 表 二、大群體與小群體埋葬蟲繁殖成功率沿環境梯度的變化 40 表 三、加熱屍體對大群體與小群體埋葬蟲繁殖成功率與總投資時間的影響 4